Periodic simple cells in cat area 17

Quantitative, high-resolution static receptive-field plots (response planes) in cat area 17 revealed simple cells whose receptive fields were composed of four to six excitatory regions alternating in space with up to seven inhibitory regions. The size, shape, and spacing of the excitatory regions within these receptive fields were highly regular, giving the receptive field a periodic appearance in space. We call these periodic simple cells. A periodic simple cell's response to moving stimuli could, in general, be anticipated from the detailed spatiotemporal map of excitatory and inhibitory regions provided by response planes. This observation suggests that periodic simple cells, like the more common simple cells composed of one to three excitatory regions, sum spatially distributed inputs in a roughly linear manner. Based on a quantitative assessment of the spatial distribution and time course of response of single excitatory regions within periodic receptive fields, as described in the previous paper, we characterized periodic simple cells as either X-like or Y-like. Furthermore, we found that periodic simple cells classified as X-like gave a more sustained response to standing contrast and had significantly smaller excitatory regions than those cells classified as Y-like. Periodic simple cells were found in layer III and at the border between layers III and IVab. It is suggested that these cells, which reside outside the primary zone of geniculate termination and include both X-like and Y-like types, may be constructed hierarchically from the convergence of lower order simple cells. In the spatial-frequency domain, periodic simple receptive fields were predicted to have bandwidths at half-maximum ranging from 0.80 to 1.4 octaves. By comparison, the predicted bandwidths of cells composed of two or three excitatory regions ranged from 1.6 to 4.3 octaves. Thus as additional excitatory regions are added to the receptive fields of simple cells, their bandwidth narrows in the spatial-frequency domain.     

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17

Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T-oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sine wave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified from fits to response temporal phase versus stimulus spatial phase data. Bicuculline reduced direction selectivity and S-T orientation in nearly all cells, and reductions in the two measures were well correlated (r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well for absolute changes in the amplitude and phase of responses to gratings drifting in the preferred and nonpreferred direction. For each cell we also calculated an exponent used to estimate the static nonlinearity. Bicuculline reduced the exponent in most cells, but the changes were not correlated with reductions in direction selectivity. We conclude that GABAA-mediated inhibition influences directional tuning in layer 4 primarily by sculpting S-T receptive-field structure. The source of the inhibition is likely to be other simple cells with certain spatiotemporal relationships to their target. Despite reductions in the two measures, most receptive fields maintained some directional tuning and S-T orientation during BMI. This suggests that their excitatory inputs, arising from the lateral geniculate nucleus and within area 17, are sufficient to create some S-T orientation and that inhibition accentuates it. Finally, BMI also reduced direction selectivity in 8 of 10 simple cells tested in layer 6, but the reductions were not accompanied by systematic changes in S-T structure. This reflects the fact that S-T orientation, as revealed by our first-order measures of the receptive field, is weak there normally. Inhibition likely affects layer 6 cells via more complex, nonlinear interactions.     

Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat.

The visual receptive fields of 213 cells in the lateral suprasylvian visual cortex (LS, or Clare-Bishop area) were studied in cats anesthetized with nitrous oxide. Eighty-one percent of the cells were directionally selective. They responded poorly to stationary stimuli flashed on or off, but gave a directionally selective response to stimuli moving through the receptive field. Most of these had a single preferred direction and an opposite null direction. They typically responded to a range of directions of stimulus movement from 45 to 90 degrees to either side of the preferred direction. Small stimuli (1-2 degrees or smaller) typically were effective and 87% of the directionally selective cells showed spatial summation. About 32% had inhibitory mechanisms which decreased the response of the cell if the stimulus exceeded a maximum size. There was little or no evidence that LS area cells were orientation selective or sensitive to variations in stimulus shape independent of size.     

Receptive-field properties of neurons in different laminae of visual cortex of the cat

1. Receptive-field properties of neurons in the different layers of the visual cortex of normal adult cats were analyzed quantitatively. Neurons were classified into one of two groups: 1) S-cells, which have discrete on- and/or off-regions in their receptive fields and possess inhibitory side bands; 2) C-cells, which do not have discrete on- and off-regions in their receptive fields but display an on-off response to flashing stimuli. Neurons of this type rarely display side-band inhibition. 2. As a group, S-cells display lower relative degrees of binocularity and are more selective for stimulus orientation than C-cells. In addition, within a given lamina the S-cells have smaller receptive fields, lower cutoff velocities, lower peak responses to visual stimulation, and lower spontaneous activity than do the C-cells. 3. S-cells in all layers of the cortex display similar orientation sensitivities, mean spontaneous discharge rates, peak response to visual stimulation, and degrees of binocularity. 4. Many of the receptive-field properties of cortical cells vary with laminar location. Receptive-field sizes and cutoff velocities of S-cells and of C-cells are greater in layers V and VI than in layers II-IV. For S-cells, preferred velocities are also greater in layers V and VI than in layers II-IV. Furthermore, C-cells in layers V and VI display high mean spontaneous discharge rates, weak orientation preferences, high relative degrees of binocularity, and higher peak responses to visual stimulation when compared to C-cells in layers II and III. 5. The receptive-field properties of cells in layers V-VI of the striate cortex suggest that most neurons that have their somata in these laminae receive afferents from LGNd Y-cells. Hence, our results suggest that afferents from LGNd Y-cells may play a major part in the cortical control of subcortical visual functions.     

Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells

Cells in the cat's dorsal lateral geniculate nucleus (LGN) were studied by presentation of visual stimuli and also by simultaneous recording of their ganglion cell inputs in the retina. This paper describes receptive-field properties and a new system of classification for LGN X-cells that appear to receive essentially only one excitatory retinal input. These X-cells were of two distinct classes. The visual responses of one class of cell (XS, single) replicated the basic form of the responses of a retinal X-cell. The other class of cell (XL, lagged) had responses with two remarkable features: their firing lagged 40-80 ms behind that of XS-cells or ganglion cells at response onset, and they fired anomalously at times when XS-cells or ganglion cells would not be firing. Thus, for a flashing spot, XL-cells were inhibited from firing after stimulus onset, during the time when XS-cells or retinal X-cells had an initial transient peak in firing; XL-cells generally had an anomalous peak in firing after stimulus offset, after XS-cells or retinal X-cells had stopped firing. For a moving bar, XS-cells or retinal X-cells responded primarily while the bar was in the receptive-field center, whereas most of a typical XL-cell's response occurred after the bar had left the receptive-field center. The latencies of various features in the visual responses were analyzed. For several visual response latencies, the distribution was clearly bimodal, thus objectively demonstrating the existence of two cell classes. Using only the latencies from spot and bar responses, over 90% of these single-input cells could be reliably identified as belonging to one of the two classes. The remaining cells (7 of 128) were intermediate between the two classes in some but not all respects; because they had some properties in common, these cells were kept in a separate group (XPL, partially lagged). The axons of both XS- and XL-cells could be antidromically activated from visual cortex. Cortical latencies were typically 0.7-2.0 ms for XS-cells but much longer, typically 2.4-5.0 ms, for XL-cells. It is possible that XL-cells have not previously been recognized as a separate class because cells with such long latencies have been recorded infrequently in the past. Responses to central flashing spots were more transient than those of retinal X-cells for most XS-cells and more sustained for most XL-cells.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat.

1. The visual cortex receives several types of afferents from the lateral geniculate nucleus (LGN) of the thalamus. In the cat, previous work studied the ON/OFF and X/Y distinctions, investigating their convergence and segregation in cortex. Here we pursue the lagged/nonlagged dichotomy as it applies to simple cells in area 17. Lagged and nonlagged cells in the A-layers of the LGN can be distinguished by the timing of their responses to sinusoidally luminance-modulated stimuli. We therefore used similar stimuli in cortex to search for signs of lagged and nonlagged inputs to cortical cells. 2. Line-weighting functions were obtained from 37 simple cells. A bar was presented at a series of positions across the receptive field, with the luminance of the bar modulated sinusoidally at a series of temporal frequencies. First harmonic response amplitude and phase values for each position were plotted as a function of temporal frequency. Linear regression on the phase versus temporal frequency data provided estimates of latency (slope) and absolute phase (intercept) for each receptive-field position tested. These two parameters were previously shown to distinguish between lagged and nonlagged LGN cells. Lagged cells generally have latencies > 100 ms and absolute phase lags; nonlagged cells have latencies < 100 ms and absolute phase leads. With the use of these criteria, we classified responses at discrete positions inside cortical receptive fields as lagged-like and nonlagged-like. 3. Both lagged-like and nonlagged-like responses were observed. The majority of cortical cells had only or nearly only nonlagged-like zones. In 15 of the 37 cells, however, the receptive field consisted of > or = 20% lagged-like zones. For eight of these cells, lagged-like responses predominated. 4. The distribution of latency and absolute phase across the sample of cortical simple cell receptive fields resembled the distribution for LGN cells. The resemblance was especially striking when only cells in or adjacent to geniculate recipient layers were considered. Absolute phase lags were almost uniformly associated with long latencies. Absolute phase leads were generally associated with short latencies, although cortical cells responded with long latencies and absolute phase leads slightly more often than LGN cells. 5. Cells in which a high percentage of lagged-like responses were observed had a restricted laminar localization, with all but two being found in layer 4B or 5A. Cells with predominantly nonlagged-like responses were found in all layers. 6. Lagged-like zones can not be easily explained as a result of stimulating combinations of nonlagged inputs.(ABSTRACT TRUNCATED AT 400 WORDS)     

The depth distribution of optimal stimulus orientations for neurones in cat area 17

Summary Neurones recorded during penetrations through cat area 17 as near parallel to the radial fibre bundles as possible have been quantitatively tested as to their optimal orientation. Optimal orientation within any one penetration was similar though considerable variability was observed. Histological reconstruction and other considerations showed that this variability could not be attributed to poor penetration angle or limitations of the microelectrode technique. These results confirm that neurones with similar optimal orientations are found in all cortical layers at one cortical locus, but it is difficult to reconcile the variability observed with a mosaic-like distribution of orientation across the cortical surface. The findings are consistent, however, with the assumption of a continuous distribution of orientation sensitivity across the cortical surface with considerable superimposed scatter.     

Characteristics of surround inhibition in cat area 17

 The effects of stimuli falling outside the ’classical receptive field’ and their influence on the orientation selectivity of cells in the cat primary visual cortex are still matters of debate. Here we examine the variety of effects of such peripheral stimuli on responses to stimuli limited to the receptive field. We first determined the extent of the classical receptive field by increasing the diameter of a circular patch of drifting grating until the response saturated or reached a maximum, and by decreasing the diameter of a circular mask in the middle of an extended grating, centred on the receptive field, until the cell just began to respond. These two estimates always agreed closely. We then presented an optimum grating of medium-to-high contrast filling the classical receptive field while stimulating the surround with a drifting grating that had the same parameters as the central stimulus but was varied in orientation. For all but five neurons (of 37 tested), surround stimulation produced clear suppression over some range of orientations, while none showed explicit facilitation under these conditions. For 11 cells (34% of those showing suppression), the magnitude of suppression did not vary consistently with the orientation of the surround stimulus. In the majority of cells, suppression was weakest for a surround grating oriented orthogonal to the cell’s optimum. Nine of these cells (28%) exhibited maximum inhibition at the optimum orientation for the receptive field itself, but for 12 cells (38%) there was apparent ’release’ from inhibition for surround gratings at or near the cell’s optimum orientation and direction, leaving inhibition either maximal at angles flanking the optimum (9 cells) or broadly distributed over the rest of the orientation range (3 cells). This implies the existence of a subliminal facilitatory mechanism, tightly tuned at or near the cell’s optimum orientation, extending outside the classical receptive field. For just two cells of 13 tested the preferred orientation for a central grating was clearly shifted towards the orientation of a surrounding grating tilted away from the cell’s optimum. The contrast gain for central stimulation at the optimal orientation was measured with and without a surround pattern. For nine of 25 cells tested, surround stimulation at the cell’s optimum orientation facilitated the response to a central grating of low contrast (≤0.1) but inhibited that to a higher-contrast central stimulus: the contrast-response gain is reduced but the threshold contrast is actually decreased by surround stimulation. Hence the receptive field is effectively larger for low-contrast than for high-contrast stimuli. Inhibition from the periphery is usually greatest at or around the cell’s optimum, while suppression within the receptive field has been shown to be largely non-selective for orientation. Inhibition by orientations flanking the optimum could serve to sharpen orientation selectivity in the presence of contextual stimuli and to enhance orientational contrast; and it may play a part in orientation contrast illusions. Received: 28 July 1996 / Accepted: 30 January 1997     

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

Summary 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.     

Nonlinearity of spatial summation in simple cells of areas 17 and 18 of cat visual cortex.

1. Nonlinearity of spatial summation in areas 17 and 18 of cat visual cortex was compared with the type of spatial nonlinearity that differentiates X and Y cells in the lateral geniculate nucleus (LGN) and retina. The comparisons were made to examine to what extent the information from X and Y cells may remain separated in higher visual centers. 2. Responses of simple cells in areas 17 and 18 were recorded while stationary, optimally oriented sinewave gratings were sinusoidally modulated within the receptive field of the cell. Both the spatial frequency and spatial phase of the stimulus were varied. 3. Y cells in the retina and LGN are defined by the presence of a specific form of spatial nonlinearity. When tested with contrast-modulated sinewave gratings of spatial frequencies about three-fold greater than the optimal, their responses are dominated by a frequency-doubled component. The amplitude of the frequency-doubled component is not dependent on the spatial phase of the stimulus. 4. Many simple cells in the cortex showed a form of spatial nonlinearity similar to the defining nonlinearity found in retinal and geniculate Y cells. A frequency-doubled response dominated at spatial frequencies more than threefold greater than the optimal spatial frequency. When this response was present, it was phase independent. 5. More than 50% of the simple cells in area 18 showed the Y-like spatial nonlinearity. Fewer than 10% of the simple cells in area 17 showed the Y-like spatial nonlinearity. 6. The virtual absence of Y-like nonlinearity in area 17 and its relative abundance in area 18 suggest that the functional separation between the parallel X and Y pathways remains distinct within areas 17 and 18 of cat visual cortex.     

Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys

Response properties of single neurons in the middle temporal visual area (MT) of anesthetized owl monkeys were determined and quantified for flashed and moving bars of light under computer control for position, orientation, direction of movement, and speed. Receptive-field sizes, ranging from 4 to 25 degrees in width, were considerably larger than receptive fields with corresponding eccentricities in the striate cortex. Neurons were highly binocular with most cells equally or nearly equally activated by either eye. Neurons varied in selectivity for axis and direction of moving bars. Some neurons demonstrated little or no selectivity, others were bidirectional on a single axis, while the largest group was highly selective for direction with little or no response to bar movement opposite to the preferred direction. Over 70% of neurons were classified as highly selective and 90% showed some preference for direction and/or axis of stimulus movement. Neurons typically responded to bar movement only over a restricted range of velocities. The majority of neurons responded best to a particular velocity within the 5-60 degrees/s range, with marked attenuation of the response for velocities greater or less than the preferred. Some neurons failed to show significant response attenuation even at the lowest tested velocity, while other neurons preferred velocities of 100 degrees/s or more and failed to attenuate to the highest velocities. Response magnitude varied with stimulus dimensions. Increasing the length of the moving bar typically increased the magnitude of the response slightly until the stimulus exceeded the receptive-field borders. Other neurons responded less to increases in bar length within the excitatory receptive field. Neurons preferred narrow bars less than 1 degree in width, and marked reductions in responses characteristically occurred with wider stimuli. Moving patterns of randomly placed small dots were often as effective as or more effective than single bars in activating neurons. Selectivity for direction of movement remained for the dot pattern. for the dot pattern. Poststimulus time (PST) histograms of responses to bars flashed at a series of 21 different positions across the receptive field, in the "response-plane" format, indicated a spatially and temporally homogeneous receptive-field structure for nearly all neurons. Cells characteristically showed transient excitation at both stimulus onset and offset for all effective stimulus locations. Some cells responded mainly at bright stimulus onset or offset.     

Regional and laminar distribution of choline acetyltransferase immunoreactivity in the cat superior colliculus

The pattern of distribution of cholinergic fibers was examined immunohistochemically in the cat superior colliculus by using a monoclonal antibody against choline acetyltransferase (ChAT). In the superficial layers, an obvious immunoreactive zone was found in the rostral two-thirds of the outer portion of the superficial gray layer (SGS), with increasing immunoreactive intensity at the rostral pole of the colliculus. A mesh-like distribution of the immunoreactive fibers was found throughout the deeper portion of this layer with a higher concentration in the caudal levels. In the deeper collicular layers, a number of ChAT-immunoreactive fibers were seen in the outer portion of the intermediate gray layer (SGI) in a patch-like fashion. A few fibers were also immunoreactive in the deeper portion of the SGI and in the medial aspect of the deep gray layer. The density of the immunoreactivity in the deeper layers increased in the caudal levels. After unilateral destruction of the parabigeminal nucleus, the ChAT immunoreactivity was markedly reduced in the rostral aspect of the contralateral SGS, and moderately in the caudal aspect of the ipsilateral SGS.     

Receptive-field properties of cells in the dorsal part of the albino rat's lateral geniculate nucleus

Receptive-field properties of 273 relay (principal, P-) cells of the dorsal lateral geniculate nucleus (LGd) were studied in urethane-anesthetized albino rats, in an attempt to see if there is some relation between the visual property and the conduction velocity of afferent optic nerve fibers. According to properties of the receptive-field center, P-cells were classified into two types, common (89%) and uncommon (11%). The common type consists of OFF-phasic, ON-phasic, ON-tonic and ON-OFF-phasic cells, while the uncommon type includes ON-inhibited, moving-sensitive, ON-OFF-inhibited, simple-cell-like and complex-cell-like cells. The mean response latency to single optic chiasm shocks increases in the order of OFF-phasic (1.94 msec), ON-phasic (2.35 msec), ON-tonic (2.87 msec), ON-OFF-phasic cells (3.04 msec) and uncommon type (3.18 msec). The mean size of the receptive-field center in each of the four common types was smaller than that in the uncommon type; 6 degrees--7 degrees vs. 11 degrees. From responsiveness to moving light spots with speeds faster than 25 degrees--30 degrees/sec, P-cells of the common type were divided into the fast- and slow-movement-sensitive cells. The ratio of occurrences of fast- to slow-movement-sensitive cells decreases in the order of the OFF-phasic (2.7), ON-phasic (2.4), ON-tonic (1.1) and ON-OFF-phasic types (0.06). The optic chiasm latencies were shorter than 2.5 msec in most of the fast-movement-sensitive cells while the reverse was true for most of the slow-movement-sensitive cells. From these findings discussions were made to point out that the rat LGd mainly consists of Y- and W-like P-cells and that the Y/W dichotomy of P-cells approximately corresponds to the previously established fast/slow classification.     

Orientational influences of layer V of visual area 18 upon cells in layer V of area 17 in the cat cortex

We examined the orientation tuning curves of 86 cells located in layer V of area 17, before, during, and after focal blockade of a small (300-m diameter) region of near-retinotopic register in layer V of area 18 of quantitatively established orientation preference. Such focal blockade revealed three distinct populations of area 17 layer V cells-cells with decreased responses to stimuli of some orientations (21%), cells with increased responses to stimuli of some orientations (43%), and cells unaffected by the focal blockade (36%). These effects were clearcut, reproducible, and generally directly related to the known receptive field properties of the cell recorded in area 18 at the center of the zone of blockade. These effects were also analyzed in terms of alterations in orientation bandwidth in the cells in area 17 as a result of the blockade-bandwidth increases (22%) and decreases (24%) were found; however, these changes were essentially unrelated to the measured receptive field properties. Inhibitory and excitatory effects were most pronounced when the regions in areas 17 and 18 were of like ocular dominance and were of similar orientation preference. Inhibitory effects (suggesting a normally excitatory input) were most dependent upon the similarity of receptive fields; excitatory effects (suggesting a normally inhibitory input) were less heavily dependent.