Showing papers on "Receptive field published in 1986"

Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis

Abstract: Anatomical studies in the visual cortex have shown the presence of long-range horizontal connections with clustered axonal collaterals, suggesting interactions over distances of several millimeters. We used cross-correlation analysis in cat striate cortex to detect interactions between cells over comparable distances. Using one cell as a reference, we recorded from other cells with a second electrode at varying distances and looked for correlated firing between the two recording sites. This technique allowed us to combine a physiological measure of the strength and type of connection between cells with a characterization of their receptive field properties. The observed interactions were excitatory, and extended over horizontal distances of several millimeters. Furthermore, the interactions were between orientation columns of like specificity, resulting in a waxing and waning in the strength of interaction as the electrodes passed through different orientation columns. We studied relationships between strength of correlation and other receptive field properties and found a tendency for facilitatory interactions between cells sharing the same eye preference. A large proportion of our correlations was due to common input. This feature, and the similarity of interactions between cells in the same column with the reference cell, suggest a high degree of interconnectivity between and within the columns. As the distance between the two electrodes increased, the overlap of the receptive fields of the cells participating in the interactions gradually diminished. At the furthest distances recorded, the cell pairs had nonoverlapping receptive fields separated by several degrees. The distribution and range of these interactions corresponded to the clustering and extent of the horizontal connections observed anatomically.

Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey

Abstract: The middle temporal (MT) and medial superior temporal (MST) areas of the macaque cortex have many cells that respond to straight movements in the frontoparallel plane with directional selectivity (D cells). We examined their responses to movements of a bar, of a wide dot pattern, and to combined movements of the two in anesthetized and immobilized animals. D cells in MT showed a wide variety in the strength of the inhibitory field surrounding the excitatory center field. Responses of SI+-type cells to a bar moving across the excitatory field were suppressed when a wide dot pattern moved over the surround field in the same direction and at the same speed as the bar. Inhibition was selective to the direction and speed of the surround movement, and the effective area for inhibition occupied a wide area, which expanded in all radial directions. Responses of SI- -type cells to a center bar movement were changed little by a conjoint movement over the surround field. Consequently, SI- -type cells responded to wide-field movement as well as to stimuli confined within the excitatory field. Although D cells in MST commonly had large excitatory fields, a proportion of them (Figure type) responded to bar movement much more strongly than to wide-field movement. Their responses to a bar movement were suppressed direction-selectively by a conjoint movement of a wide dot-pattern background. The effective area for inhibition coexisted with the excitatory field in these cells. MST cells of the Nonselective type responded comparably well to the two stimuli, and those of the Field type responded much more strongly to wide-field movement than to bar movement. It is thus suggested that MT cells of the SI+ type and MST cells of the Figure type can detect a difference between movements of an object and its wide background, whereas MST cells of the Field type can detect a conjoint movement of a wide field, neglecting the movements of a single object.

Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey

Abstract: Using anesthetized and paralyzed monkeys, we have studied the visual response properties of neurons in the cortical area surrounding the middle temporal area (MT) in the superior temporal sulcus (STS). Systematic electrode penetrations revealed that there is a functionally distinct region where three classes of directionally selective cells with large receptive fields cluster. This region is anteriorly adjoined to the dorsal two-thirds of MT, has a width of 4-5 mm mediolaterally, and therefore may correspond to the dorsal part of the medial superior temporal area (MST), which was previously defined as a MT-recipient zone. One class of cells responded to a straight movement of patterns in the frontoparallel plane with directional selectivity (D cells: 217/422, 51.4%). The second class of cells selectively responded to an expanding or contracting size change of patterns (S cells: 66/422, 15.7%). These cells responded neither to a change in width of a slit of any orientation or any length, nor to a change in brightness. The third class of cells responded only to a rotation of patterns in one direction (R cells: 58/422, 13.7%). A majority of these cells (41/58) responded to the clockwise or counterclockwise rotation of patterns in the frontoparallel plane (Rf cells), while the rest responded to a rotation of patterns in depth (Rd cells). We will suggest that these cells acquire the ability to discover whole events of visual motion--i.e., unidirectional straight movement, size change (radial movement), and rotation--by integrating elemental motion information extracted by MT cells. The receptive fields of D, S, and Rf cells can be constructed by converging signals of MT cells, the preferred directions of which are arranged in parallel (D cells), radially (S cells), and circularly (Rf cells). The receptive fields of Rd cells can be constructed, in turn, by the convergence of signals of S cells.

Multiple visual areas in the caudal superior temporal sulcus of the macaque

Abstract: Anatomical and physiological evidence indicates that, in addition to area MT, much of the cortex in the caudal superior temporal sulcus (STS) of the macaque has visual functions. Yet the organization of areas outside of MT remains unclear, and there are even conflicting data on the boundaries of MT itself. To examine these issues, we recorded form neurons throughout this region in three monkeys. Anterograde or retrograde tracers were injected into MT at the conclusion of recording to identify its projection fields. Based on differences in their visuotopic organization, neuronal properties, receptive field size, myeloarchitecture, and pattern of connections with MT, several visual areas were distinguished within the caudal STS. Area MT, defined as the heavily myelinated portion of the striate (VI) projection zone in STS, contained a systematic representation of only about the central 30 degrees--40 degrees of the contralateral field. The far peripheral field was represented medial to MT in MTp, which we had previously found receives projections from far peripheral V1 and V2 (Ungerleider and Desimone: J. Comp. Neurol. 248:147-163, 1986). Like MT, MTp contained a high proportion of directionally selective cells, and receptive field size in MTp was the size expected of MT fields if the latter were to extend into the periphery. Areas MST (medial superior temporal) and PP (posterior parietal) were found medial to MT and MTp. Both MST and PP had a high proportion of directionally selective cells, but only MST received a direct projection from MT. Cells in MST had larger receptive fields than those in either MT or MTp but nonetheless displayed a crude visuotopic organization. Receptive fields of cells in PP were even larger, some including the entire contralateral visual field. Furthermore, unlike cells in MST, some in PP responded to auditory or somesthetic stimuli in addition to visual stimuli. Area FST, which has a distinctive myeloarchitecture, was found anterior to MT in the fundus of the STS, for which it is named. FST received a direct projection from MT, but only about a third of its cells were directionally selective. Receptive fields of cells in FST were large, often included the center of gaze, and often crossed into the ipsilateral visual field. Area V4t (transitional V4) and a portion of V4 were found lateral to MT within the STS, and both received direct projections from MT. V4t has a distinctive, light myelination. Both areas had a low incidence of directionally selective cells, and both contained coarse representations of the lower visual field.(ABSTRACT TRUNCATED AT 400 WORDS)

The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus.

Abstract: In the mammalian visual system, the lateral geniculate nucleus is commonly thought to act merely as a relay for the transmission of visual information from the retina to the visual cortex, a relay without significant elaboration in receptive field properties or signal strength. However, many morphological and electrophysiological observations are at odds with this view. Only 10–20% of the synapses found on geniculate relay neurons are retinal in origin. Roughly half of all synapses derive from cells in layer VI of visual cortex; roughly one third are inhibitory and GABAergic, derived either from interneurons or from cells of the nearby perigeniculate nucleus. Most of the remaining synapses probably derive from cholinergic, noradrenergic, and serotonergic sites within the brainstem reticular formation. Moreover, recent biophysical studies have revealed several ionic currents present in virtually all thalamic neurons. One is a Ca2+-dependent K+ current underlying the afterhyperpolarization (or the IAHP), which may last up to 100–200 ms following an action potential. Activation of the IAHP leads to spike frequency adaptation in response to a sustained, suprathreshold input. Intracellular recordings from other neuronal preparations have shown that the IAHP can be blocked by noradrenalin or acetylcholine, leading to an increased cellular excitability. Another ionic current results from a voltage- and time-dependent Ca2+ conductance that produces a low threshold spike. Activation of this conductance transforms a geniculate neuron from a state of faithful relay of information to one of bursting behavior that bears little relationship to the activity of its retinal afferents. We propose that state-dependent gating of geniculate relay cells, which may represent part of the neuronal substrate involved in certain forms of selective visual attention, can be effected through at least three different mechanisms: (1) conventional GABAergic inhibition, which is largely controlled via brainstem and cortical afferents through interneurons and perigeniculate cells; (2) the IAHP, which is controlled via noradrenergic and cholinergic afferents from the brainstem reticular formation; and (3) the low threshold spike, which may be controlled by GABAergic inputs, cholinergic inputs, and/or the corticogeniculate input, although other possibilities also exist. Furthermore, it seems likely that gating functions involving the corticogeniculate pathway are suited to attentional processes within the visual domain (e.g., saccadic suppression), whereas brain-stem inputs seem more likely to have more global effects that switch attention between sensory systems. In any case, it is now abundantly clear that geniculate circuitry and the intrinsic electrophysiological properties of geniculate neurons are no longer compatible with the notion that the lateral geniculate nucleus serves as a simple relay.

Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT.

Abstract: Mechanisms of direction selectivity and speed selectivity were studied in single neurons of the middle temporal visual area (MT) of behaving macaque monkeys. Visual stimuli were presented in both smooth and stroboscopic motion within a neuron's receptive field as the monkey fixated a stationary point of light. Direction selectivity, speed selectivity, and the spontaneous discharge characteristics of MT neurons in behaving monkeys were similar to those reported in previous studies in anesthetized monkeys. Stroboscopic motion stimuli were sequences of flashes characterized by the spatial and temporal intervals between each flash. The spatial and temporal intervals were systematically varied so that suppressive and facilitatory interactions could be studied in both the preferred and null directions. Suppression and facilitation were measured by subtracting the peak discharge rate elicited by a single flash from the peak discharge rate elicited by a stroboscopic train of flashes. The dominant mechanism of direction selectivity in MT was a pronounced suppression of discharge for motion in the null direction which we interpreted as inhibition. The inhibition was sufficiently potent to abolish the responses to single flashed stimuli when they were embedded in a series of flashes in the null direction, and it frequently reduced the neuronal discharge to a level below the spontaneous firing rate. Facilitation in the preferred direction was a prominent feature of the responses of some, but not all, MT neurons. The peak discharge rate for stroboscopic motion in the preferred direction was more than twice the peak rate to a single flash for approximately 50% of the neurons in our sample. The direction selectivity of most MT neurons showed the effects of both inhibitory and facilitatory mechanisms, and it was not possible to segregate MT neurons into distinct groups on the basis of these measures. Suppressive mechanisms contributed to speed tuning as well as direction tuning. The low-speed cutoff for motion in the preferred direction resulted from suppression in 82% of the neurons tested. The high-speed cutoff resulted from suppression in 32% of the neurons tested. The latter mechanism appeared to be distinct from the inhibitory mechanism which acted in the null direction in that large spatial intervals were required for its activation.

Motion selectivity in macaque visual cortex. II. Spatiotemporal range of directional interactions in MT and V1

Abstract: We measured the spatial and temporal limits of directional interactions for 105 directionally selective middle temporal (MT) neurons and 26 directionally selective striate (V1) neurons. Directional interactions were measured using sequentially flashed stimuli in which the spatial and temporal intervals between stimuli were systematically varied over a broad range. A direction index was employed to determine the strength of directional interactions for each combination of spatial and temporal intervals tested. The maximum spatial interval for which directional interactions occurred in a particular neuron was positively correlated with receptive-field size and with retinal eccentricity in both MT and V1. The maximum spatial interval was, on average, three times as large in MT as in V1. The maximum temporal interval for which we obtained directional interactions was similar in MT and V1 and did not vary with receptive-field size or eccentricity. The maximum spatial interval for directional interactions as measured with flashed stimuli was positively correlated with the maximum speed of smooth motion that yielded directional responses. MT neurons were directionally selective for higher speeds than were V1 neurons. These observations indicate that the large receptive fields found in MT permit directional interactions over longer distances than do the more limited receptive fields of V1 neurons. A functional advantage is thereby conferred on MT neurons because they detect directional differences for higher speeds than do V1 neurons. Recent psychophysical studies have measured the spatial and temporal limits for the perception of apparent motion in sequentially flashed visual displays. A comparison of the psychophysical results with our physiological data indicates that the spatiotemporal limits for perception are similar to the limits for direction selectivity in MT neurons but differ markedly from those for V1 neurons. These observations suggest a correspondence between neuronal responses in MT and the short-range process of apparent motion.

Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex.

Abstract: Neurons of the visual cortex of the cat were penetrated with intracellular electrodes and postsynaptic potentials evoked by visual stimuli recorded. By alternately polarizing the cell with steady current injected through the recording electrode, IPSPs and EPSPs could be recorded and analyzed independently. Hyperpolarizing current suppressed IPSPs and enhanced EPSPs by moving the membrane potential toward the IPSP equilibrium potential. Depolarizing the cell toward the EPSP equilibrium potential enhanced IPSP. The responses to electrical stimulation of the LGN, where EPSPs and IPSPs could be distinguished easily by virtue of their characteristic latencies and shapes, were used to set the current injection to the appropriate level to view the two types of synaptic potential. EPSPs were found to be well oriented in that maximal depolarizing responses could be evoked at only one stimulus orientation; rotating the stimulus orientation in either direction produced a fall in the EPSP response. IPSPs were also well tuned to orientation, and invariably the preferred orientations of EPSPs and IPSPs in any one cell were identical. In addition, no systematic difference in the width of tuning of the two types of potential was seen. This result has been obtained from penetrations of over 30 cortical cells, including those with simple and complex receptive fields. It is concluded that orientation of cortical receptive fields is neither created nor sharpened by inhibition between neurons with different orientation preference. The function of inhibition evoked simultaneously with excitation by optimally oriented stimuli has yet to be determined, though it is likely to be the mechanism underlying other cortical receptive field properties, such as direction selectivity and end-stopping.

Generation of end-inhibition in the visual cortex via interlaminar connections

Abstract: To understand the mechanisms by which the receptive field properties of visual cortical cells are generated, one must consider both the thalamic input to the cortex and the intrinsic cortical connections In the cat striate cortex, layer 4 is the main recipient of input from the lateral geniculate nucleus, yet the cells in that layer possess several receptive field properties that are distinct from the geniculate input, including orientation specificity, binocularity, directionality and end-inhibition, the last of which allows cells to respond to edges of a restricted length These properties could be generated by connections within the layer, by its input from the claustrum or by the massive projection that layer 4 receives from layer 6 In the present study, we attempted to determine the functional role of the layer 6 to layer 4 projection by reversible inactivation of layer 6 using the inhibitory transmitter gamma-aminobutyric acid (GABA) After inactivating layer 6, cells in layer 4 lost end-inhibition Cells in layer 2 + 3, which receive their principal input from layer 4, were similarly affected The elimination of end-inhibition was specific, other receptive field properties, such as direction selectivity or orientation specificity, remaining intact

Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat.

Abstract: Cortical neurons using the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) are known to contribute to the formation of neuronal receptive field properties in the primary visual cortex (area 17) of the cat. In order to determine the cortical location of GABA containing neurons and what proportion of cortical neurons might use GABA as their transmitter, we analysed their distribution quantitatively using a post-embedding GABA immunohistochemical method on semithin sections in conjunction with stereological procedures. The mean total numerical density of neurons in the medial bank of the lateral gyrus (area 17) of five adult cats was 54,210±634 per mm3 (¯x±SD). An average of 20.60±0.48% (¯x±SEM) of the neurons were immunoreactive for GABA. The density of GABA-immunoreactive neurons was somewhat higher in layers II, III and upper VI, compared with layers I, IV, V and lower VI, with the lowest density being in layer V. The proportion of GABA-immunopositive cells relative to immunonegative neurons gradually decreased from the pia to the white matter. Layer I was different from other layers in that approximately 95% of its neurons were GABA-immunoreactive. The results allowed the calculation of the absolute numbers of GABAergic neurons in each layer under a given cortical surface area and could provide the basis for the quantitative treatment of cortical circuits.

Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: influence of eccentricity.

Abstract: One hundred and forty two neurons in V1 and V2 were quantitatively tested using a multihistogram technique in paralyzed and anesthetized macaque monkeys. V1 neurons with receptive fields within 2 d...

Organization and post-natal development of the monkey's lateral geniculate nucleus.

Abstract: We have studied the properties of neurones in the lateral geniculate nucleus (l.g.n.) of Old World monkeys, both in mature animals and throughout post-natal development. Cells were classified as X (linear) or Y (non-linear) on the basis of their responses to contrast-reversing achromatic gratings ('null position test'). In older animals virtually all parvocellular neurones and the majority of magnocellular units were X cells; only about 15% of magnocellular neurones displayed highly non-linear spatial summation, with no 'null position', typical of Y cells. X cells could not reliably be distinguished from Y cells, nor magnocellular from parvocellular, on the basis of their temporal patterns of discharge. Some Y cells responded transiently to contrast reversal of a grating far from the receptive field but X cells showed little or no such 'shift effect'. The spatial resolution of mature l.g.n. cells varied with the eccentricity of their receptive fields such that the best of them, at each point in the visual field, resolved drifting achromatic gratings about as well as a human observer. X cells in parvocellular and magnocellular layers had similar 'acuities', even in the central foveal representation, but Y cells generally had poorer resolution. Receptive fields in the temporal retina tended to have lower resolution than those at comparable eccentricities in the nasal retina. Even on the day of birth all cells we studied responded to visual stimulation and virtually all could be classified as X or Y. The laminar distribution of cell types and the general morphological appearance of the nucleus seemed very similar to those in the adult, but neurones in very young animals had low spontaneous activity, sluggish responses, and latencies to visual stimulation longer than any we saw in the adult. Until 3 weeks of age or so, many neurones suffered cumulative 'fatigue' when visually stimulated over several minutes. Visual latency was essentially mature by about 10 weeks. In the l.g.n. of the neonatal monkey there was little variation in neuronal 'acuity' with eccentricity: even in the foveal area the best cells could resolve only about 5 cycles/deg. Over the first year or more of life there is a gradual increase in responsiveness and about a 7-fold improvement in spatial resolution for foveal l.g.n. cells, correlating roughly with the behavioural maturation of visual acuity.

Physiology and morphology of the lamina I spinomesencephalic projection.

Abstract: We have examined the physiological and morphological characteristics of spinal dorsal horn lamina I neurons with projections to the midbrain in the cat by combining physiological recording of neurons with the intracellular injection of HRP. Lamina I spinomesencephalic neurons were antidromically activated from the region that included the cuneiform nucleus and lateral periaqueductal gray at the intercollicular level. The majority of mesencephalic projection neurons (50 of 55) responded exclusively to noxious stimulation (nociceptive-specific) of their peripheral receptive fields. Lamina I spinomesencephalic neurons were activated from both the ipsilateral and contralateral midbrain and had slow antidromic conduction velocities (1 to 18 m/second). We identified eight cells with projections to both the midbrain and the thalamus and eight cells that were antidromically activated only from the thalamus. Intracellular injection of HRP revealed that lamina I spinomesencephalic neurons were of diverse morphological types, but generally had extensive, rostrocaudally oriented, dendritic arbors confined to lamina I and the overlying white matter. Axons were observed on nine of the HRP-filled spinomesencephalic neurons; five of the axons issued collateral branches. The morphological characteristics of these neurons did not appear to correlate with functional categories (i.e., wide-dynamic-range- or nociceptive-specific-type neurons). The large number of nociceptive-specific neurons with projections to the midbrain and the interconnections of these midbrain sites with hypothalamic and limbic structures suggest that the lamina I spinomesencephalic pathway plays an important role in the autonomic and affective responses to pain.

Microelectrode maps, myeloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels.

Abstract: Microelectrode mapping methods and anatomical procedures were combined in the same animals to reveal the cortical connections of three architectonically distinct representations of the body surface in the somatosensory cortex of grey squirrels. In individual experiments, microelectrode multiunit recordings were used to determine the somatotopic organization of regions of the cortex and to identify sites for injections of the anatomical tracer, wheat germ agglutinin conjugated to horseradish peroxidase. After the brains were perfused, the cortex was separated from the brainstem, flattened, and cut parallel to the flattened surface to facilitate comparisons of areal connection patterns, physiological data, and architectonic subdivisions. Recordings in the primary (S-I) and secondary (S-II) somatosensory fields confirmed earlier descriptions of the somatotopic organization of these fields (Sur et al.: J. Comp. Neurol. 179:425-450, '78; Nelson et al.: J. Comp. Neurol. 184:473-490, '79). In addition, recordings in the cortex caudal to S-I and ventral to S-II revealed a third representation of the body surface in parietal cortex, the parietal ventral area (PV). Neurons in PV were responsive to light tactile stimulation of skin and hairs. Multiple unit receptive fields of neurons in PV were larger than those for neurons in S-I but similar in size to those for neurons in S-II. PV represented the contralateral body surface in a somatotopic manner that can be roughly characterized as an inverted "homunculus" with the limbs directed medially, the trunk located ventrally, and the face congruent with the representations of the upper lip and nose in S-I. Neurons in some electrode penetrations in PV were also responsive to auditory clicks. Microlesions placed at physiologically determined borders allowed all three somatic representations to be related to myeloarchitectonically defined fields. S-I was architectonically distinct as a densely myelinated region. Within S-I, a lightly myelinated oval of the cortex between the representation of the hand and face, the "unresponsive zone" (Sur et al.: J. Comp. Neurol. 179:425-450, '78), was an easily recognized landmark. S-II and PV corresponded to less densely myelinated fields. Other subdivisions such as motor cortex, primary auditory cortex, and visual areas 17 and 18 were distinguished. Connections were revealed by placing injections within S-I, S-II, or PV.(ABSTRACT TRUNCATED AT 400 WORDS)

The structure and symmetry of simple-cell receptive-field profiles in the cat's visual cortex

Abstract: Receptive fields of simple cells in the cat visual cortex have recently been discussed in relation to the 'theory of communication' proposed by Gabor (1946). A number of investigators have suggested that the line-weighting functions, as measured orthogonal to the preferred orientation, may be best described as the product of a Gaussian envelope and a sinusoid (i.e. a Gabor function). Following Gabor's theory of 'basis' functions, it has also been suggested that simple cells can be categorized into even- and odd-symmetric categories. Based on the receptive field profiles of 46 simple cells recorded from cat visual cortex, our analysis provides a quantitative description of both the receptive-field envelope and the receptive-field 'symmetry' of each of the 46 cells. The results support the notion that, to a first approximation, Gabor functions with three free parameters (envelope width, carrier frequency and carrier phase) provide a good description of the receptive-field profiles. However, our analysis does not support the notion that simple cells generally fit into even- and odd-symmetric categories.

A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway

Abstract: The role of action potentials in the development of proper synaptic connections in the mammalian CNS was studied in the kitten retinogeniculate pathway. Our basic finding is that there is improper segregation of retinal inputs onto LGN cells after prolonged retinal action-potential blockade. Retinal ganglion cell firing was silenced from birth by repeated monocular injections of TTX. The resulting ganglion cell connections in the LGN were studied electrophysiologically after the action-potential blockade was ended. Most cells in the deprived LGN layers received excitatory input from both ON-center and OFF-center type ganglion cells, whereas LGN cells normally receive inputs only from ON-center or OFF-center ganglion cells, but not from both types. Improper segregation of ON and OFF inputs has never been reported after other types of visual deprivation that do not block ganglion cell activity. Control experiments showed that receptive fields in the nondeprived LGN layers were normal, that ganglion cell responses remained normal, and that there was no obvious ganglion cell loss. We also showed that individual LGN cells with ON and OFF excitatory inputs were not present in normal neonatal kittens. Two other types of improper input segregation in response to action-potential blockade were also found in the deprived LGN layers. (1) A greater than normal number of LGN cells received both X- and Y-type ganglion cell input. (2) Almost half of the cells at LGN layer borders were excited binocularly. Recovery of LGN normality was rapid and complete after blockade that lasted for only 3 weeks from birth, but little recovery was seen after about 11 weeks of blockade. The susceptibility to action-potential blockade decreased during the first 3 postnatal weeks. These findings may result from axon-terminal sprouting or from the failure of axon terminals to retract. The results are consistent with the idea that normally synchronous activity of neighboring ganglion cells of like center-type may be used in the refinement of retinogeniculate synaptic connections.

The binocular organization of complex cells in the cat's visual cortex

Abstract: We have studied the manner by which inputs from the two eyes are combined in complex cells of the cat's visual cortex. The stimuli are drifting sinusoidal gratings presented dichoptically at optimal spatial frequency and orientation. The relative phase between the gratings for left and right eyes is varied over 360 degrees. Approximately 40% of complex cells show phase-specific binocular interaction where response amplitudes vary depending on the relative phase of the gratings shown to the two eyes. This interaction is similar to that observed for most simple cells. We devised a test to examine whether the phase-specific interaction in complex cells results from linear convergence of neural signals at subunits of the receptive fields. The data from this test are consistent with a linear combination model. The phase-specific binocular interaction data from complex cells imply that the optimal relative phase of the receptive field subunits is closely matched. Another type of complex cell, approximately 40% of the total, could be driven through either eye, but exhibited non-phase-specific responses to dichoptically presented gratings. This type of interaction is found only in complex cells. Binocularly non-phase-specific complex cells may have subunits whose optimal relative phases are random or monocular. The division of complex cells into these two major groups (binocularly phase specific and non-phase specific) is independent of whether they are standard or special complex-cell types. A small proportion (8%) of complex cells that appear monocular by alternate tests of each eye show a purely inhibitory influence from the silent eye. This inhibition is not generally dependent on the relative phase of the gratings. Unlike simple cells, complex cells are not a homogeneous group. However, nearly half of complex cells show phase-specific binocular interaction that is probably the result of linear convergence. Combined with the results from simple cells, the majority of binocular interaction in the striate cortex may be accounted for by linear summation of neural signals from each eye. This provides a simplified view of the nature of binocular interaction in the visual cortex.

Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe

Abstract: The electrosensory lateral line lobe (ELLL) of weakly electric fish, the primary electrosensory processing station, receives a large descending input from the midbrain in addition to the input from the electroreceptor afferents. The role of a major component of this descending input in determining the properties of ELLL output neurons was investigated. The descending input was reduced or eliminated by microinjections of the local anesthetic lidocaine or by small lesions. This treatment increased the responses of the ELLL output neurons to suprathreshold stimuli by about 300% and also increased the size of the neurons' receptive fields for moving electrolocation targets and the resolution with which they encode target distance. The neurons' threshold sensitivity and tuning to amplitude modulation frequency were unchanged by removal of the descending input. The results of this study show that this portion of the descending input to the ELLL normally mediates an inhibition that controls the responsiveness of ELLL output neurons. This descending input could function as a gain control mechanism, allowing the animal to modulate the sensitivity of the electrosensory system in response to changing environmental conditions.

Microcircuitry of beta ganglion cells in cat retina

Abstract: We reconstructed from electron micrographs of 189 serial ultrathin sections a major portion of the dendritic tree of an on-beta ganglion cell through its sixth order of branching. One hundred three contacts from three cone bipolar cells were identified. Forty-seven contacts were from a single CBb1 cone bipolar. These were distributed widely over the dendritic tree but were frequently found on the slender “basal tuft” dendrites. Twenty-two additional contacts from a second CBb1 cell were found but not studied in detail. Thirty-four contacts were from a single CBb2 cone bipolar; these also were distributed widely but were primarily on the branches of the main dendritic arborization. A major portion of the dendritic tree of an off-beta cell was also reconstructed through its seventh order of branching. Thirty-five contacts from two cone bipolar cells were identified. Twenty-three contacts were from a single CBa1 cone bipolar and 12 widely distributed over the off-beta cell dendritic tree. We propose that the photopic receptive field center of a beta cell corresponds to the envelope of the receptive fields of the bipolar cells that connect it to the cones. The center response of a beta cell may be generated by a “push-pull” mechanism. For the on-beta cell there would be excitation at light on from CBb1 and disinhibition from CBb2 and the reverse at light off. For the off-beta cell there would be inhibition at light on from CBa2 and withdrawal of excitation from CBa1. Should the bipolars have antagonistic surrounds (so far reported only for CBb1), the beta cell surrounds as well as their centers might be generated by this push-pull mechanism.

Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord.

Abstract: The somatotopic organization of A- and C-afferent fibre terminals in the dorsal horn of the rat lumbar spinal cord was compared with the spatial location of second-order dorsal horn neuronal mechanoreceptive fields. The central terminal fields of the sural, saphenous, and tibial nerve were mapped by labelling the nerves with horseradish peroxidase (HRP). A previous study used the transganglionic transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) to produce a somatotopic map of high-threshold C-fibre terminal fields in lamina II (Swett and Woolf: J. Comp. Neurol. 231:66-77, '85). In the present study the terminal fields of low-threshold A beta afferents that terminate in laminae III and IV were mapped by using unconjugated HRP at prolonged survival times (72 hours). Unfixed tissue was used to increase the sensitivity of the tetramethylbenzidine reaction, thus allowing these afferent terminals to be clearly seen. The general spatial arrangement of the terminal fields in laminae III/IV closely resembled that found in lamina II in the mediolateral and rostrocaudal planes but because of a dorsoventral obliquity of the afferent terminals, the superficial and deeper fields are not in strict vertical register. The input to laminae II-IV of the dorsal horn may therefore be viewed as two horizontally arranged sheets of afferent terminals both accurately representing the skin surface, the more superficial sheet representing the high-threshold C-afferents and the deeper sheet, low-threshold A-beta afferents. The spatial organization of high-threshold A-delta afferents in laminae I and V appears to be quite different, with a transverse rather than a longitudinal orientation. To study dorsal horn cell receptive field organization two single units with mechanoreceptive fields were recorded extracellularly in each of 87 vertical tracks in the lumbar spinal cord, one unit in the superficial dorsal horn and the second in the deep dorsal horn. In general the somatotopic organization of the receptive fields of both sets of units followed that of the afferent terminal fields but there were cells with receptive fields that were anomalous relative to the recording site. No evidence of any vertical relation or columnar arrangement in receptive field size, threshold, or location on the body surface was found when comparing the two units in a pair. Furthermore, no laminar functional specialization was found, the majority of neurones having both low- and high-threshold inputs.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual properties and spatial distribution of neurones in the visual association area on the prelunate gyrus of the awake monkey.

Abstract: We have analysed, in the awake monkey (Macaca sylvana) the functional properties of 489 neurones in the prelunate visual area (PVA, largely corresponding to V4). PVA has a coarse retinotopic organization with the lower quadrant of the visual field represented along the prelunate gyrus. The visual periphery is located medio-dorsally, the central visual field laterally near (and within?) the inferior occipital sulcus and the upper quadrant latero-ventrally. The vertical meridian runs caudally within the lunate sulcus, the horizontal meridian crosses the prelunate gyrus and continues into the superior temporal sulcus. Receptive field diameters of neurones vary between 1° and 10° with increase towards the visual periphery, but are strictly confined to the contralateral visual field. 28% of the neurones showed spectral sensitivity. About half of these cells had strong spectral opponency, the other half showed only weak opponency with broader spectral response curves. 11 cells (2%) showed striking centre/surround interactions with inhibition, disinhibition or occlusion of the two mechanisms, and different spectral response ranges of the centre and the surround, respectively. 43% of the prelunate cells were responsive to various spatial features without spectral sensitivity. We distinguished on- and off-center cells (2%), direction and movement sensitive cells (10%) and cells sensitive to gratings of parallel lines within a limited range of orientations (about 10%). A special group were cells which responded strongly to stimuli which contained many contrasts (textures without specific orientations and without regular spatial arrangements) (9%). Many of these cells were specifically responsive to variations of the internal structure of such stimuli. 3% of the cells were strongly activated in connection with behaviour: 11 neurones discharged strongly when the monkey looked attentively at a human face or when he responded with facial expressions to a threatening expression of a person. Photographs of faces were not effective. Some neurones (1%) were activated in connection with eye movement. These neurones were found in the lateral part of the prelunate gyrus. Neurones with spectral or non-spectral properties were clustered within small, irregularly shaped patches of 1–4 mm diameter. It is concluded that the prelunate visual cortex, which we consider as part of area 19, is not just a “colour area”, but represents various features of the visual environment (including colour, luminance, movement, texture and behavioral significance), and relates them — through its subcortical and cortical outputs — to behaviour. The various visual cortical areas may be seen as a cooperative of several connections between visual input and behaviour output rather than as links in a hierarchical chain of perceptual and cognitive representations.

Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey.

Abstract: Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, previous studies have failed to find any physiological evidence that the superior colliculus influences visual activity in the cortex. We studied the relative contributions of the tectofugal and geniculostriate systems to the visual properties of neurons in the superior temporal polysensory area (STP) by comparing the effects of unilateral removal of striate cortex, the superior colliculus, or of both structures. In the intact monkey, STP neurons have large, bilateral receptive fields. Complete unilateral removal of striate cortex did not eliminate visual responses of STP neurons in the contralateral visual hemifield; rather, nearly half the cells still responded to visual stimuli in the hemifield contralateral to the lesion. Thus the visual properties of STP neurons are not completely dependent on the geniculostriate system. Unilateral striate lesions did affect the response properties of STP neurons in three ways. Whereas most STP neurons in the intact monkey respond similarly to stimuli in the two visual hemifields, responses to stimuli in the hemifield contralateral to the striate lesion were usually weaker than responses in the ipsilateral hemifield. Whereas the responses of many STP neurons in the intact monkey were selective for the direction of stimulus motion or for stimulus form, responses in the hemifield contralateral to the striate lesion were not selective for either motion or form. Whereas the median receptive field in the intact monkey extended 80 degrees into the contralateral visual field, the receptive fields of cells with responses in the contralateral field that survived the striate lesions had a median border that extended only 50 degrees into the contralateral visual field. Removal of both striate cortex and the superior colliculus in the same hemisphere abolished the responses of STP neurons to visual stimuli in the hemifield contralateral to the combined lesion. Nearly 80% of the cells still responded to visual stimuli in the hemifield ipsilateral to the lesion. Unilateral removal of the superior colliculus alone had only small effects on visual responses in STP. Receptive-field size and visual response strength were slightly reduced in the hemifield contralateral to the collicular lesion. As in the intact monkey, selectivity for stimulus motion or form were similar in the two visual hemifields. We conclude that both striate cortex and the superior colliculus contribute to the visual responses of STP neurons. Striate cortex is crucial for the movement and stimulus specificity of neurons in STP.(ABSTRACT TRUNCATED AT 400 WORDS)

Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse.

Abstract: The somatotopic organization of the parietal cortex of barbiturate-anesthetized, adult mice was studied using tungsten microelectrodes. A complete representation of the contralateral face and body occupying approximately 4.0-4.5 mm2 was found immediately posterior and lateral to the representation of the face in the first somatosensory area (SI). Within this second somatosensory area (SII), the following findings were made: A relatively large region is devoted to representations of the paws and face, especially the sinus hairs associated with the anterior upper lip and mystacial vibrissae. Receptive fields on these body regions are among the smallest found in SII, though larger than corresponding receptive fields in SI. In particular, vibrissae receptive fields always include at least several adjacent whiskers, and paw receptive fields always include at least two adjacent digits. In regions representing proximal body parts, receptive fields are considerably larger, may include both contralateral and ipsilateral limb or trunk surfaces, and sometimes include the entire body and face. Responses to both somatosensory and auditory stimulation were consistently found in the body (i.e., trunk and limb) representation, but rarely found in the face region. The face is represented most anteriorly, and the hindlimb and tail most posteriorly. Forepaw and hindpaw digits and anterior aspects of the face (e.g., perioral sinus hairs and the incisors) are represented laterally, while the back, caudal head, and mystacial vibrissae are represented medially. Within SII, therefore, a "musculus" can be viewed as having an upright body orientation with the face area bordering the face representation within SI. By comparison with SI, SII is characterized by a less pronounced layer IV, which is of irregular thickness and packing density, and by less uniformity in the layering of pyramidal cells in lamina V. In addition, SII is generally thicker from pia to white matter than SI. These results are in general accord with earlier findings from evoked potential studies in mice, but are at variance with recent reports in mice and rats that the mystacial vibrissae have only a minimal, or no, representation within SII. Indeed, the present findings suggest that the representation of the whiskers in SII may have a specialized function paralleling that in SI.

Neuronal responses to borders with and without luminance gradients in cat visual cortex and dorsal lateral geniculate nucleus.

Abstract: We investigated responses of neurones in cortical areas 17 and 18 and in the dorsal lateral geniculate nucleus (dLGN) of the cat to a phase shift in a moving line pattern forming a border without a luminance gradient (“subjective contour”). In both areas 17 and 18, S cells and B cells respond only slightly or not at all along the phase shift while C cells respond strongly. The response of C cells is strongest for line patterns with medium line separation and decreases with smaller and larger separation. In the dLGN the relative magnitude of neuronal responses along a phase shift is similar to that of C cells. However, C cells respond uniformly along the entire phase shift, whereas geniculate cells merely respond to individual line ends along the phase shift. In addition we compared responses along a phase shift and those to a luminance gradient formed by a dotted line whose dots were separated by the same distance as the line ends along the phase shift. S cells and B cells respond preferentially to dotted lines whereas C cells and geniculate cells respond equally well along both phase shifts and dotted lines. Possible explanations for these results in terms of receptive field structure and differences in inhibitory input to the cells are discussed. Differential neurone responses may account for the perceptual distinctness of the contours with and without luminance gradients.

Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis

Abstract: Data analyzed in this study were derived from the responses of 128 spinothalamic tract (STT) cells and 110 thalamic neurons recorded in 75 anesthetized monkeys. A k-means cluster analysis, a nonhierarchical clustering technique, was performed using the relative magnitudes of responses to a graded series of innocuous and noxious mechanical stimuli applied to the receptive field. For comparison, a parallel analysis was performed based on definitions of low-threshold (LT), wide dynamic range (WDR), and high-threshold (HT) cells used by our laboratory. For 128 STT cells, a classification scheme with three clusters was found statistically to be the best. This yielded groups of 22, 57, and 49 cells in clusters 1, 2, and 3, respectively. Cluster 1 cells were activated best by low-intensity mechanical stimuli, whereas cluster 3 cells were activated primarily by nociceptive stimuli. Cluster 2 cells had intermediate characteristics. When the classification scheme based on the cluster analysis was compared with the classification of the same neurons as LT, WDR, and HT cells, cluster 1 cells were divided into LT and WDR cells, whereas cluster 2 and 3 cells included WDR and HT cells. For 110 thalamic neurons, a classification scheme with five clusters was found statistically to be the best. Clusters 1-5 contained 25, 34, 17, 10, and 24 cells, respectively. Response characteristics of cells in each group indicated a gradual change in sensitivity to higher intensities of peripheral input from cluster 1 to 5. When this classification scheme was compared with the classification scheme previously used by our laboratory, cluster 1 cells belonged to the LT group, clusters 2 and 3 split into LT and WDR cells, and clusters 4 and 5 included WDR and HT cells. It is concluded that a classification scheme based on a cluster analysis of the responses of neurons to standardized stimuli may provide an objective and functionally meaningful way to categorize somatosensory neurons.

Excitatory and differential disinhibitory actions of acetylcholine in the lateral geniculate nucleus of the cat.

Abstract: Single neurones were recorded in the dorsal lateral geniculate nucleus (d.l.g.n.) of adult cats anaesthetized with a mixture of halothane, nitrous oxide and oxygen. The multibarrel-glass micro-electrodes were filled with sodium acetate, L-glutamate, acetylcholine (ACh), gamma-aminobutyric acid (GABA) and bicuculline. In normally innervated, spontaneously active d.l.g.n. cells, ACh and L-glutamate elicited increased firing rates. After elimination of the excitatory input from the retina by retinal photocoagulation, the effects of ACh and L-glutamate were similar. This proves that both drugs have direct excitatory effects on d.l.g.n. cells and that disinhibition is not the most prominent influence of ACh in the d.l.g.n. The excitatory action of ACh on relay cells in the d.l.g.n. was strongly influenced by barbiturates. Sub-narcotic levels of sodium pentobarbitone completely abolished the excitation by ACh while the response to L-glutamate remained unchanged. Excitation, centre-surround antagonism and periphery effects were elicited by spots of light and by large field phase-reversing gratings with and without central sparing of the receptive field area. Binocular inhibition was elicited with the phase-reversing grating presented to the non-dominant eye. After localized destruction of the retinal receptive field area, retinogeniculate excitation ceased and an isolated lateral inhibition was observed in the acutely deafferented d.l.g.n. cells. The time course and strength of this inhibition was disclosed by raising the background discharge with microiontophoretically applied L-glutamate. With increasing size of retinal lesions the strength of isolated lateral inhibition decreased exponentially. A maximal intrageniculate range of more than 1000 microns was derived from computations of the lateral extent of deafferentation in the d.l.g.n. The inhibition acted beyond the classic surround inhibition of d.l.g.n. cells and thus was named long-range lateral inhibition. Microiontophoretically applied GABA elicits a strong inhibitory effect at the d.l.g.n. cells which is antagonized by bicuculline. Centre-surround antagonism, binocular inhibition and long-range inhibition were blocked by bicuculline and thus proven to be GABAergic. Each class of inhibition was differentially influenced by microiontophoretically applied ACh. Long-range inhibition was disinhibited, centre-surround antagonism was enhanced, and binocular inhibition was not significantly changed. In contrast to ACh excitation, the disinhibitory action of ACh was not suppressed by pentobarbitone.(ABSTRACT TRUNCATED AT 400 WORDS)

Identified target-selective visual interneurons descending from the dragonfly brain

Abstract: 1. Eight large interneurons descending in the dragonfly (Aeshna umbrosa, Anax junius) ventral nerve cord from the brain to the thoracic ganglia were identified anatomically with intracellular dye injection (Fig. 3). All eight were strictly visual and responded only to movements of small patterns, such as black squares, ‘targets’, moving on a white background. 2. The target interneurons all projected from the protocerebrum at least as far as the metathoracic ganglion. Within the protocerebrum they arborized in the posterodorsal neuropil region, near the base of the circumesophageal connectives (Fig. 3). 3. The receptive fields of six of the cells were large, including most of the forward hemisphere of vision. For five of these, spiking responses were often restricted to a much smaller region within the receptive field, with stimulation of other areas yielding only subthreshold responses (Figs. 4 and 5, Table 1). 4. The pattern of selectivity for target size varied, with some neurons responding only to small targets, some showing consistent responses over a wide range of target sizes, and one preferring larger targets (Fig. 6, Table 1). 5. Five of the interneurons were directionally selective. Movement in the antipreferred direction elicited hyperpolarizing responses in two of them. Movements of large patterns, such as a checkerboard pattern covering the forward hemisphere, elicited opposite directional responses, i.e., hyperpolarizations in the preferred target direction and subthreshold depolarizations in the antipreferred direction (Fig. 7). A large pattern moving in any direction inhibited the response to target movement (Fig. 8). 6. These neurons mediate, in part, the visual control of flight orientation. I propose that they convey turning signals to the wing motor in response to objects moving relative to the animal.