1.

Responses of cortical cells from the foveal and perifoveal visual field representation in area 17 to moving contrasts were analyzed with intracellular records in anesthetized cats. These intracellularly recorded responses were normal in so far as the cells showed typical orientation/direction sensitivity and only short phasic or no responses to diffuse illumination.




2.

With slowly moving bright or dark bars, two types of responses were seen: those with a small excitatory peak and those with a wider excitatory peak. Inhibitory regions outside the excitatory peak were only seen in cells with a small excitatory area. Only very few cells showed inhibitory “flanks” preceding and following the excitation; often inhibition followed the excitation in both the forward and backward direction; sometimes it preceded it in both directions. The inhibition outside the excitatory zone practically always had “dynamic” properties, i.e. was smaller or larger in the two opposite directions of movements.




3.

All cells showed strong inhibition (IPSP's) mixed with excitation while the stimulus moved over the excitatory response field. The degree of inhibition was clearly sensitive to the direction of movement (forward or backward) of an optimally oriented moving stimulus, and could also be different at different orientation/ directions. However, the orientation dependence of intracortical inhibition was often less clear than the differences found between the two opposite directions of an optimally oriented stimulus. Inhibition was more marked during binocular than during monocular stimulation.




4.

The excitatory areas of cortical cells were mostly slightly elongated, but not systematically along the axis of optimal orientation. The diameters of the excitatory fields were similar along the optimal and the non-optimal orientation axes (mean 1.9±0.78 vs. 2.2±0.92°).




5.

It is proposed that the orientation/direction sensitivity of cortical cells is a function of intracortical inhibitory connections with direction/orientation sensitivity rather than only due to the spatial arrangement of excitatory and inhibitory on- or off-center fields. A hypothetical retino-cortical projection map is proposed and it is assumed that direction/orientation sensitive intracortical inhibition is essential for the functional properties of cortical neurones.

An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network.

Neuronal variability: non-stationary responses to identical visual stimuli

Transient broad-band stimuli that mimic in their spectrum and time waveform sounds arriving from a speaker in free space were delivered to the tympanic membranes of barbiturized cats via sealed and calibrated earphones. The full array of such signals constitutes a virtual acoustic space (VAS). The extra-cellular response to a single stimulus at each VAS direction, consisting of one or a few precisely time-locked spikes, was recorded from neurons in primary auditory cortex. Effective sound directions form a virtual space receptive field (VSRF). Near threshold, most VSRFs were confined to one quadrant of acoustic space and were located on or near the acoustic axis. Generally, VSRFs expanded monotonically with increases in stimulus intensity, with some occupying essentially all of the acoustic space. The VSRF was not homogeneous with respect to spike timing or firing strength. Typically, onset latency varied by as much as 4-5 msec across the VSRF. A substantial proportion of recorded cells exhibited a gradient of first-spike latency within the VSRF. Shortest latencies occupied a core of the VSRF, on or near the acoustic axis, with longer latency being represented progressively at directions more distant from the core. Remaining cells had VSRFs that exhibited no such gradient. The distribution of firing probability was mapped in those experiments in which multiple trials were carried out at each direction. For some cells there was a positive correlation between latency and firing probability.

The Structure of Spatial Receptive Fields of Neurons in Primary Auditory Cortex of the Cat

When Purkinje wrote the lines cited above in 1819 for his doctoral dissertation, he initiated a long period of successful visual research. His conviction, that all subjectively observed sensory phenomena should have correlates in objective physiology, remained a theoretical postulate for over 100 years. The electroretinogram, although discovered in 1865 by Holmgren [224], contributed little to these correlations, and objective visual physiology did not begin until 60 years later. The first successful recordings obtained from the vertebrate optic nerve by Adrian and R. Matthews in 1927 [4] and from single optic fibres by Hartline in 1935 [191] mark the pioneer steps. In 1938 followed Hartline’S classification of the responses from single optic nerve fibres in the frog [192] and of their receptive fields. Thereafter, the physiology of visual neurones made such rapid progress that it can now provide objective correlates for many visual phenomena, such as brightness, contrast and colour, on the basis of single neurone recordings from the retina, the optic nerve, and the visual projections in the brain itself.

Visual Perception and Neurophysiology

Quantitative techniques were used to demonstrate cortical layer differences in cutaneous receptive fields (RF's) in the rat SI cortex. Two- and three-dimensional (2-D and 3-D) RF maps were constructed showing the responsiveness of single neurons to standardized punctate stimulation of each of a matrix of points on the skin or the mystacial vibrissa pad. These allowed a visualization not only of the overall sizes of such RF's, but also their shape and “response profile”. Initial experiments showed that the sizes and response profiles of such RF's were similar whether they were mapped by sinusoidal mechanical vibration of skin, punctate touch, or direct intracutaneous electrical stimulation. This method was used to quantitatively determine distoproximal lengths of RF's of single units recorded at different depths in the forepaw area of the SI cortex. Plots of these RF lengths as a function of cortical depth showed that the smallest RF's were found in the granular layers (IV and deep III). RF's up to double that size were found in supragranular layers, and up to triple that size in infragranular layers. 3-D maps of RF's in the granular layers showed sharp central response peaks surrounded by very steep dropoffs to the RF boundaries. In the whisker areas, granular layer RF's were typically circular in shape and contained from 1–4 whiskers. By contrast, in supragranular layers they were often elongated in shape, and were oriented along rows or columns of whiskers. RF's in layer V resembled large, high plateaus, often supporting clearly separated peaks. RF's mapped in the fore- and hindpaw areas were similar, but, even in the granular layers, were often slightly elongated along the limb axis. In all regions of the SI, both the locations and shapes of the granular layer RF's appeared to be conserved as subsets of other more topographically heterogeneous RF's encountered elsewhere in the column. These findings may correlate with patterns of axonal connectivity in the rat SI.

Laminar differences in sizes, shapes, and response profiles of cutaneous receptive fields in the rat SI cortex.

1.

A general purpose, digital computer was employed to map quantitatively the receptive fields of units in cat's striate cortex.




2.

Receptive fields were studied as a function of barbiturate anesthetic level under dark adapted conditions.




3.

Receptive fields obtained from lateral geniculate axons were topographically simple and usually represented a single peak with concentric zones of decreasing excitability. Such fields were stable under all anesthetic and electroencephalographic conditions.




4.

Responses were recorded from striate cells, both simple and complex in the sense of Hubel and Wiesel. These demonstrated varied field configurations such as an excitatory cylinder in an inhibitory field, excitatory vertical axis flanked by asymmetric inhibitory areas, and more complex patterns including potentially direction and velocity sensitive ones.




5.

Many cortical maps were unstable over time, especially in the presence of low voltage, fast electroencephalographic activity. Changes were not random nor did they represent simple linear displacements of peaks, but included axis shifts, gradient change, and expansion or contraction of excitatory and inhibitory zones with centers at fixed relative positions.




6.

Heavy barbiturate anesthesia and spontaneous spindling in the EEG markedly reduced the variability in these maps; the encephale isole preparation was more stable than spinally intact animals. This association suggests a role of the midbrain reticular formation in cortical variability.




7.

Random rather than iterative presentation of matrix points resulted in higher mean firing rates and more stable receptive fields, probably the result of photochemical recovery in dispersed receptors and time averaging of cellular excitability.




8.

When stability was analyzed as a function of time interval of response (early on, late on, early off, late off), initial on responses were often more stable than longer latency late on- or off-responses. This factor, among others discussed, makes eye movement an unlikely explanation for map variability. It suggests additionally that late on- and off- responses represent input to the cortical cell from units other than those producing the early on-response.




9.

The effects of pentobarbital, in addition to stabilization of the receptive field, included striking phase reversals in which inhibitory regions became excitatory and visa versa. Firing rate often changed substantially, but both increases and decreases were observed.




10.

It is argued that visual response under pentobarbital is a special and not the general case of visual perception and that sequential receptive field changes during aroused brain states reflect integrative, purposive processes at the cortical level.

Sequential change in receptive fields of striate neurons in dark adapted cats

1.

A digital computer was employed to map quantitatively the receptive fields of units in cats' striate cortex. The computer presented point visual stimuli via a digital oscilloscope, synchronously sampled unit spike response, and composed a post stimulus time-histogram of response at each stimulated matrix point.




2.

Animals were prepared under diethyl ether anesthesia, immobilized with a mixture of gallamine triethiodide and d-tubocurarine, and lightly anesthetized with pentobarbital sodium. Light and dark adapted conditions were contrasted in terms of effect on organization of striate receptive fields.




3.

Striate response was analyzed temporally by means of post stimulus time-histograms. Phasic early on-, phasic late on-, tonic on-, phasic early off-, and phasic late off-response components were distinguished. The mechanism, differential behavior in light and dark adapted conditions, and functional significance of these components were investigated.




4.

From unit response at all stimulated positions, an explicit temporal interval was chosen to coincide with each discrete component of response. Net firing rate during this interval was represented as a terrain value at appropriate spatial coordinates; a contour generating program was then employed to construct a continuous surface of excitability or “fractional receptive field map.” Quantitative spatial representation of successive components of response allowed for afferent “circuit analysis” and functional predictions of moving border and contrast sensitivity.




5.

The qualitative categories of simple and complex striate unit are analyzed in the light of quantitatively determined receptive field maps. It is suggested that the distinction is not a fundamental one, but that there exists a continuum of complexity between geniculate-dominated and cortically-dominated striate units. Quantitative point stimulation appears to be an adequate and most general way of characterizing “complex” units.




6.

Receptive fields obtained under light and dark adapted conditions are contrasted with the aid of firing rate, latency, and synchronicity maps. In summary, it was the case that processes observed at the ganglion and geniculate cell level were expressed and emphasized cortically. Functional changes in striate response led to an enhancement of contrast perception and spatial acuity in light adapted conditions and the development of absolute sensitivity at the cost of resolution in darkness.

Quantitative variation in striate receptive fields of cats as a function of light and dark adaptation.

A quantitative approach to characterization of unit response in the visual system was proposed. Temporal parameters of response were analyzed by post stimulus time-histograms obtained from point visual stimulation. Explicit temporal intervals were chosen to coincide with discrete response components. By calculating net firing rate within these intervals as a function of stimulus position, quantitative receptive field maps were constructed. To estimate response between stimulated matrix mesh points, a general contouring program was described. Latency, and synchronicity — a logarithmic probability function sensitive to temporal consistency of response — were also mapped as functions of stimulus position. Representative firing rate maps morphologically resembled previously described receptive fields; latency and synchronicity maps, it is argued, allow for additional mechanistic and functional analysis of striate units. By explicitly separating temporal and spatial variables and quantifying unit response, the present methods will hopefully enlarge the scope and sensitivity of receptive field analysis.

Hideo Sasaki

Papers

Sequential change in receptive fields of striate neurons in dark adapted cats

Quantitative variation in striate receptive fields of cats as a function of light and dark adaptation.

Quantitative characterization of unit response in the visual system.