Showing papers on "Receptive field published in 1996"

Emergence of simple-cell receptive field properties by learning a sparse code for natural images

Abstract: The receptive fields of simple cells in mammalian primary visual cortex can be characterized as being spatially localized, oriented and bandpass (selective to structure at different spatial scales), comparable to the basis functions of wavelet transforms. One approach to understanding such response properties of visual neurons has been to consider their relationship to the statistical structure of natural images in terms of efficient coding. Along these lines, a number of studies have attempted to train unsupervised learning algorithms on natural images in the hope of developing receptive fields with similar properties, but none has succeeded in producing a full set that spans the image space and contains all three of the above properties. Here we investigate the proposal that a coding strategy that maximizes sparseness is sufficient to account for these properties. We show that a learning algorithm that attempts to find sparse linear codes for natural scenes will develop a complete family of localized, oriented, bandpass receptive fields, similar to those found in the primary visual cortex. The resulting sparse image code provides a more efficient representation for later stages of processing because it possesses a higher degree of statistical independence among its outputs.

A relationship between behavioral choice and the visual responses of neurons in macaque MT

Abstract: We have previously documented the exquisite motion sensitivity of neurons in extrastriate area MT by studying the relationship between their responses and the direction and strength of visual motion signals delivered to their receptive fields. These results suggested that MT neurons might provide the signals supporting behavioral choice in visual discrimination tasks. To approach this question from another direction, we have now studied the relationship between the discharge of MT neurons and behavioral choice, independently of the effects of visual stimulation. We found that trial-to-trial variability in neuronal signals was correlated with the choices the monkey made. Therefore, when a directionally selective neuron in area MT fires more vigorously, the monkey is more likely to make a decision in favor of the preferred direction of the cell. The magnitude of the relationship was modest, on average, but was highly significant across a sample of 299 cells from four monkeys. The relationship was present for all stimuli (including those without a net motion signal), and for all but the weakest responses. The relationship was reduced or eliminated when the demands of the task were changed so that the directional signal carried by the cell was less informative. The relationship was evident within 50 ms of response onset, and persisted throughout the stimulus presentation. On average, neurons that were more sensitive to weak motion signals had a stronger relationship to behavior than those that were less sensitive. These observations are consistent with the idea that neuronal signals in MT are used by the monkey to determine the direction of stimulus motion. The modest relationship between behavioral choice and the discharge of any one neuron, and the prevalence of the relationship across the population, make it likely that signals from many neurons are pooled to form the data on which behavioral choices are based.

Geometric determinants of the place fields of hippocampal neurons

Abstract: The human hippocampus has been implicated in memory, in particular episodic or declarative memory. In rats, hippocampal lesions cause selective spatial deficits, and hippocampal complex spike cells (place cells) exhibit spatially localized firing, suggesting a role in spatial memory, although broader functions have also been suggested. Here we report the identification of the environmental features controlling the location and shape of the receptive fields (place fields) of the place cells. This was done by recording from the same cell in four rectangular boxes that differed solely in the length of one or both sides. Most of our results are explained by a model in which the place field is formed by the summation of gaussian tuning curves, each oriented perpendicular to a box wall and peaked at a fixed distance from it.

Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area

Abstract: 1. Posterior parietal cortex contains neurons that are visually responsive and active in relation to saccadic eye movements. We recorded from single neurons in a subregion of parietal cortex, the lateral intraparietal area (LIP), in alert rhesus monkeys. To characterize more completely the circumstances under which LIP neurons are responsive, we used five tasks designed to test the impact of sensory, motor, and cognitive factors. We obtained quantitative data in multiple tasks in 91 neurons. We measured neural activity during central fixation and in relation to stimulus onset and saccade onset. 2. LIP neurons have visual responses to the onset of a stationary stimulus in the receptive field. These visual responses occurred both in tasks that require a subsequent eye movement toward the stimulus and in tasks in which eye movements are not permitted, indicating that this activity is sensory rather than presaccadic. 3. Visual responses were enhanced when the monkey had to use information provided by the stimulus to guide its behavior. The amplitude of the sensory response to a given stimulus was increased in a task in which the monkey would subsequently make a saccade to the location signaled by the stimulus, as compared with the amplitude of the visual response in a simple fixation task. 4. The visual response was also enhanced when the monkey attended to the stimulus without looking at it. This result shows that enhancement does not reflect saccade preparation because the response is enhanced even when the monkey is not permitted to make a saccade. Instead, enhancement reflects the allocation of attention to the spatial locus of the receptive field. 5. Many LIP neurons had saccade-related activity in addition to their visual responses. The visual response for most neurons was stronger than the saccade-related activation. 6. Saccade-related activity was independent of visual activity. Similar presaccadic activity was observed in trials that included a recent visual stimulus (memory-guided saccade task) and in trials with no visual stimulus (learned saccade task). 7. We observed increases in activity during fixation in tasks in which the monkey could anticipate the onset of a behaviorally significant stimulus. LIP neurons usually showed low levels of background firing in the fixation task during the period before stimulus onset. This background activity was increased in the peripheral attention and memory-guided saccade tasks during the period when the monkey was waiting for a behaviorally relevant stimulus to appear. 8. The results from these several tasks indicate that LIP neurons are activated in a variety of circumstances and are not involved exclusively in sensory processing or motor planning. The modulation of sensory responses by attention and anticipation suggests that cognitive factors play a major role in parietal function.

Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search.

Abstract: 1. The latency between the appearance of a popout search display and the eye movement to the oddball target of the display varies from trial to trial in both humans and monkeys. The source of the delay and variability of reaction time is unknown but has been attributed to as yet poorly defined decision processes. 2. We recorded neural activity in the frontal eye field (FEF), an area regarded as playing a central role in producing purposeful eye movements, of monkeys (Macaca mulatta) performing a popout visual search task. Eighty-four neurons with visually evoked activity were analyzed. Twelve of these neurons had a phasic response associated with the presentation of the visual stimulus. The remaining neurons had more tonic responses that persisted through the saccade. Many of the neurons with more tonic responses resembled visuomovement cells in that they had activity that increased before a saccade into their response field. 3. The visual response latencies of FEF neurons were determined with the use of a Poisson spike train analysis. The mean visual latency was 67 ms (minimum = 35 ms, maximum = 138 ms). The visual response latencies to the target presented alone, to the target presented with distractors, or to the distractors did not differ significantly. 4. The initial visual activation of FEF neurons does not discriminate the target from the distractors of a popout visual search stimulus array, but the activity evolves to a state that discriminates whether the target of the search display is within the receptive field. We tested the hypothesis that the source of variability of saccade latency is the time taken by neurons involved in saccade programming to select the target for the gaze shift. 5. With the use of an analysis adapted from signal detection theory, we determined when the activity of single FEF neurons can reliably indicate whether the target or distractors are present within their response fields. The time of target discrimination partitions the reaction time into a perceptual stage in which target discrimination takes place, and a motor stage in which saccade programming and generation take place. The time of target discrimination occurred most often between 120 and 150 ms after stimulus presentation. 6. We analyzed the time course of target discrimination in the activity of single cells after separating trials into short, medium, and long saccade latency groups. Saccade latency was not correlated with the duration of the perceptual stage but was correlated with the duration of the motor stage. This result is inconsistent with the hypothesis that the time taken for target discrimination, as indexed by FEF neurons, accounts for the wide variability in the time of movement initiation. 7. We conclude that the variability observed in saccade latencies during a simple visual search task is largely due to postperceptual motor processing following target discrimination. Signatures of both perceptual and postperceptual processing are evident in FEF. Procrastination in the output stage may prevent stereotypical behavior that would be maladaptive in a changing environment.

Orientation selectivity of thalamic input to simple cells of cat visual cortex

Abstract: MORE than 30 years after Hubel and Wiesel1 first described orientation selectivity in the mammalian visual cortex, the mechanism that gives rise to this property is still controversial. Hubel and Wiesel1 proposed a simple model for the origin of orientation tuning, in which the circularly symmetrical receptive fields of neurons in the lateral geniculate nucleus that excite a cortical simple cell are arranged in rows. Since this model was proposed, several experiments2–6 and neuronal simulations7,8 have suggested that the connectivity between the lateral geniculate nucleus and the cortex is not well organized in an orientation-specific fashion, and that orientation tuning arises instead from extensive interactions within the cortex. To test these models we have recorded visually evoked synaptic potentials in simple cells while cooling the cortex9, which largely inactivates the cortical network, but leaves geniculate synaptic input functional. We report that the orientation tuning of these potentials is almost unaffected by cooling the cortex, in agreement with Hubel and Wiesel's original proposal1.

A primate genesis model of focal dystonia and repetitive strain injury I. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys

Abstract: In this study we tested a neuroplasticity/learning origins hypothesis for repetitive strain injuries (RSIs), including occupationally induced focal dystonia.Repetitive movements produced in a specific form and in an appropriate behavioral context cause a degradation of the sensory feedback information controlling fine motor movements, resulting in the ``learned99 genesis of RSIs. Two adult New World owl monkeys were trained at a behavioral task that required them to maintain an attended grasp on a hand grip that repetitively and rapidly (20 msec) opened and closed over short distances. The monkeys completed 300 behavioral trials per day (1,100 to 3,000 movement events) with an accuracy of 80 to 90%. A movement control disorder was recorded in both monkeys. Training was continued until the performance accuracy dropped to below 50%. We subsequently conducted an electrophysiologic mapping study of the representations of the hand within the primary somatosensory (SI) cortical zone. The hand representation in the true primary somatosensory cortical field, SI area 3b, was found to be markedly degraded in these monkeys, as characterized by (1) a dedifferentiation of cortical representations of the skin of the hand manifested by receptive fields that were 10 to 20 times larger than normal, (2) the emergence of many receptive fields that covered the entire glabrous surface of individual digits or that extended across the surfaces of two or more digits, (3) a breakdown of the normally sharply segregated area 3b representations of volar glabrous and dorsal hairy skin of the hand, and (4) a breakdown of the local shifted-overlap receptive field topography of area 3b, with many digital receptive fields overlapping the fields of neurons sampled in cortical penetrations up to more than four times farther apart than normal. Thus, rapid, repetitive, highly stereotypic movements applied in a learning context can actively degrade cortical representations of sensory information guiding fine motor hand movements. This cortical plasticity/learning-based dedifferentiation of sensory feedback information from the hand contributes to the genesis of occupationally derived repetitive strain injuries, including focal dystonia of the hand. Successful treatment of patients with RSI will plausibly require learning-based restoration of differentiated representations of sensory feedback information from the hand. NEUROLOGY 1996;47: 508-520

Precisely correlated firing in cells of the lateral geniculate nucleus.

Abstract: Simple cells within layer IV of the cat primary visual cortex are selective for lines of a specific orientation. It has been proposed that their receptive-field properties are established by the pattern of connections that they receive from the lateral geniculate nucleus (LGN) of the thalamus. Thalamic inputs, however, represent only a small proportion of the synapses made onto simple cells, and others have argued that corticocortical connections are likely to be important in shaping simple-cell response properties. Here we describe a mechanism that might be involved in selectively strengthening the effect of thalamic inputs. We show that neighbouring geniculate neurons with overlapping receptive fields of the same type (on-centre or off-centre) often fire spikes that are synchronized to within 1 millisecond. Moreover, these neurons often project to a common cortical target neuron where synchronous spikes are more effective in evoking a postsynaptic response. We propose that precisely correlated firing within a group of geniculate neurons could serve to reinforce the thalamic input to cortical simple cells.

Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey.

Abstract: In visual areas of the cerebral cortex, most neurons exhibit preferences for particular features of visual stimuli, but in general, the tuning is broad. Thus, even simple stimuli evoke responses in numerous neurons with differing but overlapping feature preferences, and it is commonly held that a particular feature is encoded in the pattern of graded responses of the activated population rather than in the optimal responses of individual cells. To decipher this population code, responses evoked by a particular stimulus need to be identified and bound together for further joint processing and must not be confounded with responses to other, nearby stimuli. Such selection of related responses could be achieved by synchronizing the respective discharges at a time scale of milliseconds, as this would selectively and jointly enhance their saliency. This hypothesis predicts that a given set of neurons should exhibit synchronized discharges more often when responding to a single stimulus than when activated by different but simultaneously presented stimuli. To test this prediction, recordings were performed with two electrodes from spatially segregated cells in the middle temporal area (MT) of the awake behaving macaque monkey. It was found that cells with overlapping receptive fields, but different preferences for directions of motion, can engage in synchronous activity if they are stimulated with a single moving bar. In contrast, if the same cells are activated with two different bars, each moving in the direction preferred by the cells at the two respective sites, responses show no or much fewer synchronous epochs. Control experiments exclude that this effect is attributable to changes in response amplitude, the mere presence of two stimuli, or the specific orientation of the bars. The critical variable determining the strength of correlation is the extent to which both sites are activated by a common stimulus or by two different stimuli with different directions of motion.

Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey.

Abstract: 1. We studied the responses of 103 neurons in visual area V4 of anesthetized macaque monkeys to two novel classes of visual stimuli, polar and hyperbolic sinusoidal gratings. We suspected on both theoretical and experimental grounds that these stimuli would be useful for characterizing cells involved in intermediate stages of form analysis. Responses were compared with those obtained with conventional Cartesian sinusoidal gratings. Five independent, quantitative analyses of neural responses were carried out on the entire population of cells. 2. For each cell, responses to the most effective Cartesian, polar, and hyperbolic grating were compared directly. In 18 of 103 cells, the peak response evoked by one stimulus class was significantly different from the peak response evoked by the remaining two classes. Of the remaining 85 cells, 74 had response peaks for the three stimulus classes that were all within a factor of 2 of one another. 3. An information-theoretic analysis of the trial-by-trial responses to each stimulus showed that all but two cells transmitted significant information about the stimulus set as a whole. Comparison of the information transmitted about each stimulus class showed that 23 of 103 cells transmitted a significantly different amount of information about one class than about the remaining two classes. Of the remaining 80 cells, 55 had information transmission rates for the three stimulus classes that were all within a factor of 2 of one another. 4. To identify cells that had orderly tuning profiles in the various stimulus spaces, responses to each stimulus class were fit with a simple Gaussian model. Tuning curves were successfully fit to the data from at least one stimulus class in 98 of 103 cells, and such fits were obtained for at least two classes in 87 cells. Individual neurons showed a wide range of tuning profiles, with response peaks scattered throughout the various stimulus spaces; there were no major differences in the distributions of the widths or positions of tuning curves obtained for the different stimulus classes. 5. Neurons were classified according to their response profiles across the stimulus set with two objective methods, hierarchical cluster analysis and multidimensional scaling. These two analyses produced qualitatively similar results. The most distinct group of cells was highly selective for hyperbolic gratings. The majority of cells fell into one of two groups that were selective for polar gratings: one selective for radial gratings and one selective for concentric or spiral gratings. There was no group whose primary selectivity was for Cartesian gratings. 6. To determine whether cells belonging to identified classes were anatomically clustered, we compared the distribution of classified cells across electrode penetrations with the distribution that would be expected if the cells were distributed randomly. Cells with similar response profiles were often anatomically clustered. 7. A position test was used to determine whether response profiles were sensitive to precise stimulus placement. A subset of Cartesian and non-Cartesian gratings was presented at several positions in and near the receptive field. The test was run on 13 cells from the present study and 28 cells from an earlier study. All cells showed a significant degree of invariance in their selectivity across changes in stimulus position of up to 0.5 classical receptive field diameters. 8. A length and width test was used to determine whether cells preferring non-Cartesian gratings were selective for Cartesian grating length or width. Responses to Cartesian gratings shorter or narrower than the classical receptive field were compared with those obtained with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the four cells that had shown significant preferences for non-Cartesian gratings in the main test, none showed tuning for Cartesian grating length or width that would account for their non-Cartesian res

Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis

Abstract: Auditory cortical receptive field plasticity produced during behavioral learning may be considered to constitute "physiological memory" because it has major characteristics of behavioral memory: associativity, specificity, rapid acquisition, and long-term retention. To investigate basal forebrain mechanisms in receptive field plasticity, we paired a tone with stimulation of the nucleus basalis, the main subcortical source of cortical acetylcholine, in the adult guinea pig. Nucleus basalis stimulation produced electroencephalogram desynchronization that was blocked by systemic and cortical atropine. Paired tone/nucleus basalis stimulation, but not unpaired stimulation, induced receptive field plasticity similar to that produced by behavioral learning. Thus paired activation of the nucleus basalis is sufficient to induce receptive field plasticity, possibly via cholinergic actions in the cortex.

Estimation of self-motion by optic flow processing in single visual interneurons.

Abstract: Humans, animals and some mobile robots use visual motion cues for object detection and navigation in structured surroundings Motion is commonly sensed by large arrays of small field movement detectors, each preferring motion in a particular direction Self-motion generates distinct 'optic flow fields' in the eyes that depend on the type and direction of the momentary locomotion (rotation, translation) To investigate how the optic flow is processed at the neuronal level, we recorded intracellularly from identified interneurons in the third visual neuropile of the blowfly The distribution of local motion tuning over their huge receptive fields was mapped in detail The global structure of the resulting 'motion response fields' is remarkably similar to optic flow fields Thus, the organization of the receptive fields of the so-called VS neurons strongly suggests that each of these neurons specifically extracts the rotatory component of the optic flow around a particular horizontal axis Other neurons are probably adapted to extract translatory flow components This study shows how complex visual discrimination can be achieved by task-oriented preprocessing in single neurons

Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis (receptive field plasticityyauditory cortexyassociative learning)

Abstract: Auditory cortical receptive field plasticity produced during behavioral learning may be considered to constitute''physiologicalmemory''becauseithasmajorchar- acteristics of behavioral memory: associativity, specificity, rapid acquisition, and long-term retention. To investigate basal forebrain mechanisms in receptive field plasticity, we pairedatonewithstimulationofthenucleusbasalis,themain subcortical source of cortical acetylcholine, in the adult guinea pig. Nucleus basalis stimulation produced electroen- cephalogram desynchronization that was blocked by systemic and cortical atropine. Paired toneynucleus basalis stimula- tion, but not unpaired stimulation, induced receptive field plasticity similar to that produced by behavioral learning. Thus paired activation of the nucleus basalis is sufficient to induce receptive field plasticity, possibly via cholinergic ac- tions in the cortex.

Excitatory synaptic inputs to spiny stellate cells in cat visual cortex

Abstract: In layer 4 of cat visual cortex, the monocular, concentric receptive fields of thalamic neurons, which relay retinal input to the cortex, are transformed into 'simple' cortical receptive fields that are binocular and selective for the precise orientation, direction of motion, and size of the visual stimulus. These properties are thought to arise from the pattern of connections from thalamic neurons, although anatomical studies show that most excitatory inputs to layer 4 simple cells are from recurrently connected circuits of cortical neurons. We examined single fibre inputs to spiny stellate neurons. We examined single fibre inputs to spiny stellate neurons in slices of cat visual cortex, and conclude that thalamocortical synapses are powerful and the responses they evoke are unusually invariant for central synapses. However, the responses to intracortical inputs, although less invariant, are strong enough to provide most of the excitation to simple cells in vivo. Our results suggest that the recurrent excitatory circuits of cortex may amplify the initial feedforward thalamic signal, subserving dynamic modifications of the functional properties of cortical neurons.

Representation and integration of multiple sensory inputs in primate superior colliculus.

Abstract: 1. The properties of visual-, auditory-, and somatosensory-responsive neurons, as well as of neurons responsive to multiple sensory cues (i.e., multisensory), were examined in the superior colliculus of the rhesus monkey. Although superficial layer neurons responded exclusively to visual stimuli and visual inputs predominated in deeper layers, there was also a rich nonvisual and multisensory representation in the superior colliculus. More than a quarter (27.8%) of the deep layer population responded to stimuli from more than a single sensory modality. In contrast, 37% responded only to visual cues, 17.6% to auditory cues, and 17.6% to somatosensory cues. Unimodal- and multisensory-responsive neurons were clustered by modality. Each of these modalities was represented in map-like fashion, and the different representations were in alignment with one another. 2. Most deep layer visually responsive neurons were binocular and exhibited poor selectivity for such stimulus characteristics as orientation, velocity, and direction of movement. Similarly, most auditory-responsive neurons had contralateral receptive fields and were binaural, but had little frequency selectivity and preferred complex, broad-band sounds. Somatosensory-responsive neurons were overwhelmingly contralateral, high velocity, and rapidly adapting. Only rarely did somatosensory-responsive neurons require distortion of subcutaneous tissue for activation. 3. The spatial congruence among the different receptive fields of multisensory neurons was a critical feature underlying their ability to synthesize cross-modal information. 4. Combinations of stimuli could have very different consequences in the same neuron, depending on their temporal and spatial relationships. Generally, multisensory interactions were evident when pairs of stimuli were separated from one another by < 500 ms, and the products of these interactions far exceeded the sum of their unimodal components. Whether the combination of stimuli produced response enhancement, response depression, or no interaction depended on the location of the stimuli relative to one another and to their respective receptive fields. Maximal response enhancements were observed when stimuli originated from similar locations in space (as when derived from the same event) because they fell within the excitatory receptive fields of the same multisensory neurons. If, however, the stimuli were spatially disparate such that one fell beyond the excitatory borders of its receptive field, either no interaction was produced or this stimulus depressed the effectiveness of the other. Furthermore, maximal response interactions were seen with the pairing of weakly effective unimodal stimuli. As the individual unimodal stimuli became increasingly effective, the levels of response enhancement to stimulus combinations declined, a principle referred to as inverse effectiveness. Many of the integrative principles seen here in the primate superior colliculus are strikingly similar to those observed in the cat. These observations indicate that a set of common principles of multisensory integration is adaptable in widely divergent species living in very different ecological situations. 5. Surprisingly, a few multisensory neurons had individual receptive fields that were not in register with one another. This has not been noted in multisensory neurons of other species, and these "anomalous" receptive fields could present a daunting problem: stimuli originating from the same general location in space cannot simultaneously fall within their respective receptive fields, a stimulus pairing that may result in response depression. Conversely, stimuli that originate from separate events and disparate locations (and fall within their receptive fields) may result in response enhancement. However, the spatial principle of multisensory integration did not apply in these cases. (ABSTRACT TRUNCATED)

Spatial integration and cortical dynamics

Abstract: Cells in adult primary visual cortex are capable of integrating information over much larger portions of the visual field than was originally thought. Moreover, their receptive field properties can be altered by the context within which local features are presented and by changes in visual experience. The substrate for both spatial integration and cortical plasticity is likely to be found in a plexus of long-range horizontal connections, formed by cortical pyramidal cells, which link cells within each cortical area over distances of 6-8 mm. The relationship between horizontal connections and cortical functional architecture suggests a role in visual segmentation and spatial integration. The distribution of lateral interactions within striate cortex was visualized with optical recording, and their functional consequences were explored by using comparable stimuli in human psychophysical experiments and in recordings from alert monkeys. They may represent the substrate for perceptual phenomena such as illusory contours, surface fill-in, and contour saliency. The dynamic nature of receptive field properties and cortical architecture has been seen over time scales ranging from seconds to months. One can induce a remapping of the topography of visual cortex by making focal binocular retinal lesions. Shorter-term plasticity of cortical receptive fields was observed following brief periods of visual stimulation. The mechanisms involved entailed, for the short-term changes, altering the effectiveness of existing cortical connections, and for the long-term changes, sprouting of axon collaterals and synaptogenesis. The mutability of cortical function implies a continual process of calibration and normalization of the perception of visual attributes that is dependent on sensory experience throughout adulthood and might further represent the mechanism of perceptual learning.

Encoding of binocular disparity by simple cells in the cat's visual cortex

Abstract: 1. Spatiotemporal receptive fields (RFs) for left and right eyes were studied for simple cells in the cat's striate cortex to examine the idea that stereoscopic depth information is encoded via structural differences of RFs between the two eyes. Traditional models are based on neurons that possess matched RF profiles for the two eyes. We propose a model that requires a subset of simple cells with mismatched RF profiles for the two eyes in addition to those with similar RF structure. 2. A reverse correlation technique, which allows a rapid measurement of detailed RF profiles in the joint space-time domains, was used to map RFs for isolated single neurons recorded extracellularly in the anesthetized paralyzed cat. 3. Approximately 30% of our sample of cells shows substantial differences between spatial RF structure for the two eyes. Nearly all of these neurons prefer orientations between oblique and vertical, and are therefore presumed to be involved in processing horizontal disparities. On the other hand, cells that prefer orientations near horizontal have matched RF profiles for the two eyes. Considered together, these findings suggest that the visual system takes advantage of the orientation anisotropy of binocular disparities present in the retinal images. 4. For some cells, the spatial structure of the RF changes over the time course of the response (inseparable RF in the space-time domain). In these cases, the change is similar for the two eyes, and therefore the difference remains nearly constant at all times. Because the difference of the RF structure between the two eyes is the critical determinant of a cell's relative depth selectivity for the proposed model, space-time inseparability of RFs is not an obstacle for consistent representation of stereoscopic information. 5. RF parameters including amplitude, RF width, and optimal spatial frequency are generally well matched for the two eyes over the time course of the response. The preferred speed and direction of motion are also well matched for the two eyes. These results suggest that the encoding of motion in depth is not likely to be a function of simple cells in the striate cortex. 6. The results presented here are consistent with our model, in which stereoscopic depth information is encoded via differences in the spatial structure of RFs for the two eyes. This model provides a natural binocular extension of the current notion of monocular spatial form encoding by a population of simple cells. Note, however, that our findings do not exclude the possibility that positional shifts of RFs also play a role in determining the disparity selectivity of cortical neurons.

Responses in Area V4 Depend on the Spatial Relationship Between Stimulus and Attention

Abstract: 1. We studied the spatial interaction between stimulus and attention in macaque area V4. Monkeys were required to fixate a small spot while continuously attending to a ring-shaped target within a large array of identical rings. Meanwhile, the response of the V4 cell under study was tested by flashing behaviorally irrelevant bar stimuli in the cell's classical receptive field (CRF). The location of the attended ring was varied across four positions surrounding the CRF, and the location of the bar stimulus was varied across five positions spanning the CRF. 2. Response strength depended on two aspects of the spatial relationship between the stimulus driving the cell (the bar) and the position of attention (the target ring). First, for 49% of the cells studied, responses were greater for bar stimuli near the attended ring; i.e., the receptive field profile shifted toward the attentional focus. Second, for 84% of the cells, the overall response level depended on the direction in which attention lay relative to the stimulus in the CRF (e.g., to the left, right, above, or below). 3. This study confirms a key prediction of spatial models of attention, which postulate enhanced processing of all stimuli near the attentional focus. It also introduces the novel finding that responses are influenced by the relative direction of attention. This result indicates that area V4 carries information about the spatial relationship between visual stimuli and attention.

The Representation of Brightness in Primary Visual Cortex

Abstract: Although neurons in primary visual cortex are sensitive to the spatial distribution and intensity of light, their responses have not been thought to correlate with the perception of brightness. Indeed, primary visual cortex is often described as an initial processing stage that sends information to higher cortical areas where perception of brightness, color, and form occurs. However, a significant percentage of neurons in primary visual cortex were shown to respond in a manner correlated with perceived brightness, rather than responding strictly to the light level in the receptive fields of the cells. This finding suggests that even at the first stage of visual cortical processing, spatial integration of information yields perceptual qualities that are only indirectly related to the pattern of illumination of the retina.

Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey

Abstract: We have compared physiological data recorded from three alert macaque monkeys with separate observations of local connectivity, to locate and characterize the functional border between two related but distinct visual areas on the caudal face of the superior parietal gyrus. We refer to these areas as V6 and V6A. The occupy almost the entire extent of the anterior bank of the parieto-occipital sulcus, V6A being the more dorsal. These two areas are strongly interconnected. Anatomically, we have defined the border as the point at which labelled axon terminals first adopt a recognizably 'descending' pattern in their laminar characteristics, after injections of wheatgerm agglutinin-horseradish peroxidase into the dorsal half of the gyrus (in presumptive V6A). A similar principle was used to recognize the same border by the pattern of input from area V5, except that in this case the relevant transition in laminar characteristics is that between an 'intermediate' pattern (in V6) and an 'ascending' pattern (in V6A). V6A was found to be distinct from V6 in a number of its physiological properties. Unlike V6, it contains visually unresponsive cells as well as units with craniotopic receptive fields ('real-position' cells), units tuned to very slow stimulus speeds, units with complex visual selectivities and units with activity related to attention. V6A was also found to have a larger mean receptive field size and scatter than V6. By contrast, response properties related to the basic orientation and direction of moving bar stimuli were indistinguishable between V6 and V6A, as was the influence of gaze direction on cell activity in the two areas. Two-dimensional maps of the recording sites allowed reconstruction of the V6/V6A border. For comparison, the anatomical results were rendered on two-dimensional maps of identical format to those used to summarize the physiological data. After normalizing for relative size, the physiological and connectional estimates of the border between V6 and V6A were found to coincide, at least within the range of individual variation between hemispheres. An architectonic map in the same format was also made from a hemisphere stained for myelin and Nissl substance. Area PO, defined by its general density of myelination was not distinct in this material, but several architectural features were traceable and one of these was also found to approximate the V6/V6A border. The particular criteria that distinguish V6 from V6A differ from a recent description of areas PO and POd in the Cebus monkey; we believe it most likely that PO and POd together may correspond to V6.

Processing of color, form, and motion in macaque area V2.

Abstract: We investigated the representation of color in cortical area V2 of macaque monkeys, and the association of color with other stimulus attributes. We measured the selectivity of individual V2 neurons for color, motion, and form. Most neurons in V2 were orientation selective, about half of them were selective for color, and a minority of cells (about 20%) were selective for size or direction. We correlated these physiological measurements with the anatomical location of the cells with respect to the cytochrome oxidase (CO) compartments of area V2. There was a tendency for color-selective cells to be found more frequently in the thin stripes, but color-selective cells also occurred frequently in thick stripes and inter-stripes. We found no difference in the degree of color selectivity between the different CO compartments. Furthermore, there was no negative correlation between color selectivity and selectivity for other stimulus attributes. We found many cells capable of encoding information along more than one stimulus dimension, regardless of their location with respect to the CO compartments. We suggest that area V2 plays an important role in integrating information about color, motion, and form. By this integration of stimulus attributes a cue-invariant representation of the visual world might be achieved.

The Functional Organization of Local Circuits in Visual Cortex: Insights from the Study of Tree Shrew Striate Cortex

Abstract: We have used a combination of anatomical and physiological techniques to explore the functional organization of vertical and horizontal connections in tree shrew striate cortex. Our studies of vertical connections reveal a remarkable specificity in the laminar arrangement of the projections from layer IV to layer III that establishes three parallel intracortical pathways. The pathways that emerge from layer IV are not simple continuations of parallel thalamocortical pathways. Layer IV and its connections with layer II/III restructure the inputs from the LGN, combining the activity from ON and OFF channels and from the left and right eye and transmit the products of this synthesis to separate strata within the overlying layers. In addition, studies of two other prominent vertical connection pathways, the projections from layer VI to layer IV and from layer II/III to layer V suggest that the parallel nature of these systems is perpetuated throughout the cortical depth. Our studies of horizontal connections have revealed a systematic relationship between a neuron's orientation preference and the distribution of its axon arbor across the cortical map of visual space. Horizontal connections in layer II/III extend for greater distances and give rise to a greater number of terminals along an axis of the visual field map that corresponds to the neuron's preferred orientation. These findings suggest that the contribution of horizontal inputs to the response properties of layer II/III neurons is likely to be greater in regions of visual space that lie along the axis of preferred orientation (endzones) than along the orthogonal axis (side zones). Topographically aligned horizontal connections may contribute to the orientation preference of layer II/III neurons and could account for the axial specificity of some receptive field surround effects. Together, these results emphasize that specificity in the spatial arrangement of local circuit axon arbors plays an important role in shaping the response properties of neurons in visual cortex.

Multineuronal codes in retinal signaling

Abstract: The visual world is presented to the brain through patterns of action potentials in the population of optic nerve fibers. Single-neuron recordings show that each retinal ganglion cell has a spatially restricted receptive field, a limited integration time, and a characteristic spectral sensitivity. Collectively, these response properties define the visual message conveyed by that neuron's action potentials. Since the size of the optic nerve is strictly constrained, one expects the retina to generate a highly efficient representation of the visual scene. By contrast, the receptive fields of nearby ganglion cells often overlap, suggesting great redundancy among the retinal output signals. Recent multineuron recordings may help resolve this paradox. They reveal concerted firing patterns among ganglion cells, in which small groups of nearby neurons fire synchronously with delays of only a few milliseconds. As there are many more such firing patterns than ganglion cells, such a distributed code might allow the retina to compress a large number of distinct visual messages into a small number of optic nerve fibers. This paper will review the evidence for a distributed coding scheme in the retinal output. The performance limits of such codes are analyzed with simple examples, illustrating that they allow a powerful trade-off between spatial and temporal resolution.

Circuitry for color coding in the primate retina

Abstract: Human color vision starts with the signals from three cone photoreceptor types, maximally sensitive to long (L-cone), middle (M-cone), and short (S-cone) wavelengths. Within the retina these signals combine in an antagonistic way to form red-green and blue-yellow spectral opponent pathways. In the classical model this antagonism is thought to arise from the convergence of cone type-specific excitatory and inhibitory inputs to retinal ganglion cells. The circuitry for spectral opponency is now being investigated using an in vitro preparation of the macaque monkey retina. Intracellular recording and staining has shown that blue-ON/yellow-OFF opponent responses arise from a distinctive bistratified ganglion cell type. Surprisingly, this cone opponency appears to arise by dual excitatory cone bipolar cell inputs: an ON bipolar cell that contacts only S-cones and an OFF bipolar cell that contacts L- and M-cones. Red-green spectral opponency has long been linked to the midget ganglion cells, but an underlying mechanism remains unclear. For example, receptive field mapping argues for segregation of L-and M-cone signals to the midget cell center and surround, but horizontal cell interneurons, believed to generate the inhibitory surround, lack opponency and cannot contribute selective L- or M-cone input to the midget cell surround. The solution to this color puzzle no doubt lies in the great diversity of cell types in the primate retina that still await discovery and analysis.

Subthreshold facilitation and suppression in primary visual cortex revealed by intrinsic signal imaging.

Abstract: Neurons in primary visual cortex (area 17) respond vigorously to oriented stimuli within their receptive fields; however, stimuli presented outside the suprathreshold receptive field can also influence their responses. Here we describe a fundamental feature of the spatial interaction between suprathreshold center and subthreshold surround. By optical imaging of intrinsic signals in area 17 in response to a stimulus border, we show that a given stimulus generates activity primarily in iso-orientation domains, which extend for several millimeters across the cortical surface in a manner consistent with the architecture of long-range horizontal connections in area 17. By mapping the receptive fields of single neurons and imaging responses from the same cortex to stimuli that include or exclude the aggregate suprathreshold receptive field, we show that intrinsic signals strongly reveal the subthreshold surround contribution. Optical imaging and single-unit recording both demonstrate that the relative contrast of center and surround stimuli regulates whether surround interactions are facilitative or suppressive: the same surround stimulus facilitates responses when center contrast is low, but suppresses responses when center contrast is high. Such spatial interactions in area 17 are ideally suited to contribute to phenomena commonly regarded as part of "higher-level" visual processing, such as perceptual "popout" and "filling-in."

Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels

Abstract: 1. Carbon fiber multibarrel glass microelectrodes were used to record extracellular single-unit activity during microiontophoretic application of gamma-aminobutyric acid (GABA) or bicuculline methiodide (BMI) onto layer IV barrel neurons in the somatosensory cortex of fentanyl-sedated rats. Excitatory and inhibitory aspects of the neurons' receptive fields were quantified with the use of controlled whisker stimuli. The principally activating whisker and one of its immediately adjacent neighbors were deflected alone or in paired combinations involving a condition-test paradigm. 2. Units were distinguished electrophysiologically on the basis of the time course of their action potential waveforms. Data were obtained from 26 regular-spike units (RSUs; presumed spiny stellate cells) and 7 fast-spike units (FSUs; presumed GABAergic neurons). An average of 15.0 nA of GABA produced a one-third to one-half reduction in RSU responses evoked by the maximally effective stimulus. An average of 8.7 nA of BMI was needed to counteract this reduction. This amount of BMI, in the absence of exogenous GABA, was found to increase average RSU and FSU responses by 98 and 53%, respectively, relative to predrug levels. 3. For RSUs, the BMI-induced twofold increase in responses evoked by moving the principal whisker at the neuron's best deflection angle was accompanied by an almost threefold increase in responses evoked by similarly moving an adjacent whisker. Disproportionately large percentage increases were also seen for responses to nonpreferred directions of principal and adjacent whisker movement. BMI thus effectively increased receptive field size and decreased angular tuning. Similarly, responses to stimulus offsets, which are normally smaller than ON responses, were increased proportionally more. 4. Predrug responses of FSUs were more vigorous than those of RSUs. However, FSUs showed a similar inverse relationship between percentage increase with BMI and initial response magnitude, although the proportional increases were less pronounced. 5. GABA, like BMI, had the greatest proportional effects on those responses that were initially smallest. It produced results opposite those of BMI, effectively decreasing receptive field size and sharpening angular tuning. 6. A previously described computational model of a barrel was tested for its ability to reproduce quantitatively the effects of BMI and GABA. The application of BMI was simulated by decreasing the strength of the inhibitory inputs onto the particular cell under study in the model network. GABA microiontophoresis was simulated by adding a constant hyperpolarizing voltage. The model RSUs and FSUs displayed proportional changes in response magnitude that were quantitatively similar to those of their biological counterparts. 7. Surround inhibition was greatly attenuated by BMI application, both for the real and simulated barrel neurons. Disinhibition was less pronounced for the former, perhaps because, unlike the simulated neurons, they also possess GABAB receptors, which are unaffected by BMI. 8. We conclude that the inhibitory receptive field properties of barrel neurons can be explained by intrabarrel inhibition and that the expansion of receptive field size and loss of angular tuning with BMI is due to an enhanced effectiveness of convergent, multi-whisker thalamocortical input. Examination of the model neurons' behavior suggests that the altered activity in response to GABA or BMI application, respectively, can be explained by the nonlinear effects of shifting somal membrane potential away from or toward the neuron's firing threshold.

Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus.

Abstract: We studied the relationship between the morphology of ganglion cells and the spatial density of photoreceptors in the retina of two Old World primates, human and macaque monkey; the diurnal New World marmoset Callithrix jacchus; and the cat Ganglion cells in macaque and marmoset were labelled by intracellular injection with Neurobiotin or by DiI diffusion labelling in fixed tissue Cone photoreceptor densities were measured from the same retinas Supplemental data for macaque and data for human and cat were taken from published studies For the primates studied, the central retina is characterised by a constant numerical convergence of cones to ganglion cells Midget ganglion cells derive their input, via a midget bipolar cell, from a single cone Parasol cells derive their input from 40-140 cones Outside the central retina, the convergence increases with eccentricity The convergence to beta cells in the cat retina is very close to that for parasol cells in primate retina The convergence of rod photoreceptors to ganglion cells is similar in human, macaque, and marmoset, with parasol cells receiving input from 10-15 times more rods than midget cells The low convergence of cones to midget cells in human and macaque retinas is associated with distinctive dendritic "clusters" in midget cells' dendritic fields Convergence in marmoset is higher, and the clusters are absent We conclude that the complementary changes in photoreceptor density and ganglion cell morphology should be considered when forming linking hypotheses between dendritic field, receptive field, and psychophysical properties of primate vision