Receptive fields and response properties of neurons in layer 4 of ferret visual cortex

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 +/- 1.2 degrees (mean +/- SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.     

Contrast affects speed tuning, space-time slant, and receptive-field organization of simple cells in macaque V1

We measured speed tuning of V1 cells in alert macaques to high- and low-contrast stimuli. Most V1 cells tested, both simple and complex and directional as well as nondirectional, shifted their speed tuning to slower speeds for lower contrast stimuli. We found that the space-time slant of the receptive field of directional simple cells differed for high- and low-contrast stimuli, with the space-time slant predicting higher optimum speeds for the higher-contrast stimuli; i.e., there was a larger spatial shift of the receptive-field organization per unit time. Not only did the space-time maps of directional simple cells show different slants between high- and low-contrast stimuli, but they also showed a different organization, because for high-contrast stimuli, the maps tended to show a complete inversion of the receptive-field spatial organization at long delays after stimulus onset, with initial excitation followed by suppression and initial suppression followed by excitation, but for low-contrast stimuli the receptive-field organization showed only a quadrature shift over time. We show that a simple modification of earlier models for the generation of direction-selective simple cells can account for these observations.     

Laminar processing of stimulus orientation in cat visual cortex

One of the most salient features to emerge in visual cortex is sensitivity to stimulus orientation. Here we asked if orientation selectivity, once established, is altered by successive stages of cortical processing. We measured patterns of orientation selectivity at all depths of the cat's visual cortex by making whole-cell recordings with dye-filled electrodes. Our results show that the synaptic representation of orientation indeed changes with position in the microcircuit, as information passes from layer 4 to layer 2+3 to layer 5. At the earliest cortical stage, for simple cells in layer 4, orientation tuning curves for excitation (depolarization) and inhibition (hyperpolarization) had similar peaks (within 0–7 deg,   n = 11  ) and bandwidths. Further, the sharpness of orientation selectivity covaried with receptive field geometry (   r = 0.74  ) - the more elongated the strongest subregion, the shaper the tuning. Tuning curves for complex cells in layer 2+3 also had similar peaks (within 0–4 deg,   n = 7  ) and bandwidths. By contrast, at a later station, layer 5, the preferred orientation for excitation and inhibition diverged such that the peaks of the tuning curves could be as far as 90 deg apart (average separation, 54 deg;   n = 6  ). Our results support the growing consensus that orientation selectivity is generated at the earliest cortical level and structured similarly for excitation and inhibition. Moreover, our novel finding that the relative tuning of excitation and inhibition changes with laminar position helps resolve prior controversy about orientation selectivity at later phases of processing and gives a mechanistic view of how the cortical circuitry recodes orientation.     

Direction selectivity of simple cells in the primary visual cortex: comparison of two alternative mathematical models. I: response to drifting gratings

Two models of a single hypercolumn in the primary visual cortex are presented, and used for the analysis of direction selectivity in simple cells. The two models differ as to the arrangement of inhibitory connections: in the first ("antiphase model") inhibition is in phase opposition with excitation, but with a similar orientation tuning; in the second ("in-phase model"), inhibition is in phase with excitation, but with broader orientation tuning. Simulation results, performed by using drifting gratings with different orientations, and different spatial and temporal frequencies, show that both models are able to explain the origin of direction preference of simple cells.     

Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat

1. The orientation tuning of lateral geniculate nucleus (LGN) neurons and retinal ganglion cells (recorded as S potentials in the LGN) was investigated with drifting grating stimuli. 2. Results were compared with a quantitative model, in which receptive fields were constructed from linear, elliptical Gaussian center and surround subunits, and responses could be predicted to gratings of any spatial frequency at any orientation. 3. The orientation tuning of X and Y retinal ganglion cells and LGN neurons was shown to result from the linear mechanism of receptive-field elongation, as data from these cells could be well fit with this model. 4. The responses of LGN neurons and their input retinal ganglion cells were compared. The orientation tuning of LGN neurons was found to be a reflection of the tuning of their retinal inputs, showing that neither intrageniculate neural interactions nor the corticogeniculate projection play any role in LGN orientation selectivity.     

Spatial receptive-field properties of direction-selective neurons in cat striate cortex

Responses of direction-selective neurons in cat striate cortex (area 17) were studied with flashed-bar stimuli. Spatial parameters of interactions within the receptive field giving rise to direction selectivity and of receptive-field subunits were quantitatively determined for the same cells and correlated. A bar stimulus flashed sequentially at two nearby locations in the receptive field produced direction-selective behavior comparable with that elicited by continuously moving stimuli. Each cell exhibited a characteristic optimal spatial displacement, Dopt, for which responses in the presumed preferred and null directions were maximally distinct. In all cases, Dopt was much smaller than the receptive-field size. The spatial structure of receptive fields in simple cells was studied using single narrow-bar stimuli flashed at different locations in the receptive field. The resulting line-weighting function exhibited alternating regions of ON and OFF responses having a characteristic spatial period or wavelength, lambda. Spatial subunit structure in complex cells was determined by flashing two bars simultaneously in the receptive field. The response as a function of bar separation was again a wavelike function having a spatial wavelength, lambda. Values of the optimal displacement for direction selectivity, Dopt, showed a clear relationship with the spatial wavelength, lambda, for a given unit. Dopt was also correlated to a somewhat lesser degree with receptive-field size. Generally, the ratio of Dopt to lambda was approximately 1/10 to 1/4, in agreement with theoretical predictions by Marr and Poggio. Taken together with the findings of Movshon et al., these results indicate a systematic relationship between Dopt and the spatial frequency of a sinusoidal grating, which is optimal for that cell. Such a relationship is consistent with the results of human psychophysical experiments on apparent motion.     

Response properties of visual cortical neurons in cats reared in stroboscopic illumination

1. The response properties of 182 units were studied in the primary visual cortices (155 in area 18 and 27 in area 17) in eight cats reared from birth in a stroboscopically illuminated environment (frequency, 2/s; duration, 200 microseconds). Multihistogram quantitative testing was carried out in 82 units (64 in area 18 and 18 in area 17). Two hundred three neurons recorded and quantitatively tested in areas 17 and 18 of the normal adult cat were used for comparison. 2. Spatial characteristics of receptive fields investigated using hand-held stimuli were found to be abnormal. The correlation between receptive-field width and eccentricity was lost in area 18 and consequently, receptive fields were significantly wider in area 18 subserving central vision. Cells could be classified according to the spatial characteristics of their receptive fields. There was a much smaller proportion of end-stopped cells in strobe-reared animals. Orientation tuning in the deprived animals was normal except for a small number of cells that showed no selectivity for stimulus orientation. 3. Compilation of velocity-response curves made it possible to classify areas 17 and 18 neurons into four categories: velocity low-pass, velocity broad-band, velocity tuned, and velocity high-pass cells. The proportion of velocity high-pass cells was reduced in area 18 subserving peripheral vision, as was the proportion of velocity-tuned cells in area 18 subserving central vision. 4. In the strobe-reared animal velocity sensitivity was somewhat different from that of the normal animal. Neurons in area 18 subserving the peripheral visual field failed to respond to fast velocities. Neurons in area 17 subserving the central visual field in strobe-reared animals responded to slightly higher velocities than in the normal animal. 5. In the deprived animals the number of neurons that were selective to the direction of motion was strongly reduced. The majority of neurons failed to show a selectivity for direction at all velocities. A number of neurons could be directional at some velocities but were unreliable, since they inverted their preferred direction with velocity changes. 6. Binocular convergence onto visual cortical cells was perturbed. In area 18 the majority of neurons were driven by the contralateral eye. In area 17 most neurons could be driven only by either the ipsilateral or contralateral eye. 7. Quantitative testing (of direction selectivity, sensitivity to high velocities, response latency, and strength) and qualitative testing (receptive-field width, end stopping, and ocular dominance) showed that the normal influence of eccentricity on functional properties was strongly reduced by strobe rearing.     

Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells

The relationship between orientation selectivity and spatial receptive field organization was analyzed. Receptive field maps were made with a dual stimulus technique where an optimally oriented activation slit was presented in the most responsive region to produce activity against which the effect of a test spot in various positions was determined. Both simple and complex cells had receptive fields which were subdivided into adjacent elongated and antagonistic subregions. When the two stimuli were presented in phase (both ON or OFF simultaneously) the fields had a central enhancement region with a strong suppression flank on one or both sides. Optimal slit orientation was related to the location of the suppression flank relative to the location of the central enhancement region, and the degree of orientation selectivity to the shape of the subregions and the distance between them. Estimated orientation tuning curves calculated from the receptive field maps gave satisfactory first approximations to experimental curves. The relative contribution of enhancement and suppression to orientation selectivity was studied by presenting a test slit in different orientations in phase with an optimally oriented activation slit. The orientation selectivity was produced almost exclusively by the flank suppression indicating that orientation selectivity is produced by inhibitory input. The flank suppression lacked any specific orientation selectivity, and it occurred only when both the central region and the flanks were activated in phase. Orientation selectivity in both simple and complex cells is explained by a receptive field organization where the cells have input from partially overlapping excitatory and inhibitory fields which have their centers slightly displaced from each other.     

The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat''s striate cortex

1. The GABA antagonist bicuculline has been applied to hypercomplex cells in layers II and III of the cat's striate cortex in an attempt to test the hypothesis that their length preference derives from the action of a GABA mediated post-synaptic inhibitory input.2. Iontophoretic application of bicuculline to these cells resulted in a reduction but not an elimination of the length preference. The reduction in length preference was only observed in the case of slits extended to one side of the receptive field or to slits only partially covering what appeared to be inhibitory flanking regions either side of the field centre. In cells normally showing a clear and stable length preference it was never possible to produce by the application of bicuculline a significant response to a slit fully extended to cover both flanking regions.3. The orientation tuning was basically eliminated by the application of bicuculline. In contrast the directional specificity was relatively unaffected.4. The action of bicuculline on hypercomplex cell orientation tuning supports the view that GABA mediated inhibitory inputs were effectively blocked and suggests that the partial effect on length preference and lack of effect on directional specificity reflect the varying degree of involvement of a GABA mediated inhibitory input to these receptive field properties.5. These observations introduce the possibility that the excitatory input to the superficial layer hypercomplex cells exhibits directional specificity, length preference with respect to a slit extended to both sides of the field and a low degree of orientation selectivity. Evidence is presented indicating that certain layer V cells with hypercomplex type receptive field properties exhibit some of the characteristics required of this input.     

Cat area 17. III. Response properties and orientation anisotropies of corticotectal cells

The receptive field properties of antidromically identified corticotectal (CT) cells in area 17 were explored in the paralyzed, anesthetized cat. To compare these with another population of infragranular cells, we also examined the receptive field properties of cells in layer 6. Sixty percent of our sample of CT cells showed increased response to increased stimulus length (length summation) and were classified as standard complex cells. The other 40% showed little or no length summation, were generally end stopped, and were classified as special complex cells. Standard and special complex CT cells have complementary orientation anisotropies: the distribution of orientation preferences of standard complex cells is biased toward obliquely oriented stimuli, whereas special complex cells are biased toward horizontally and vertically oriented stimuli. The receptive fields of the cells in our sample were primarily along the horizontal meridian so we cannot determine if these anisotropies are defined relative to the vertical meridian or relative to the meridian passing through the receptive field. The effects of these anisotropies in preferred orientation are minimized by the broad orientation tuning of CT cells. There was no simple relationship between the direction bias of CT cells and the reported direction bias of tectal cells. In contrast to the heterogeneity of corticotectal cells, layer 6 cells uniformly showed strong length summation, tight orientation tuning, and little spontaneous activity.     

Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex

1. We consider the consequences of the orientation selectivity shown by most cortical neurons for the nature of the signals they can convey about the direction of stimulus movement. On theoretical grounds we distinguish component direction selectivity, in which cells are selective for the direction of movement of oriented components of a complex stimulus, from pattern direction selectivity, or selectivity for the overall direction of movement of a pattern irrespective of the directions of its components. We employed a novel test using grating and plaid targets to distinguish these forms of direction selectivity. 2. We studied the responses of 280 cells from the striate cortex and 107 cells from the lateral suprasylvian cortex (LS) to single sinusoidal gratings to determine their orientation preference and directional selectivity. We tested 73 of these with sinusoidal plaids, composed of two sinusoidal gratings at different orientations, to study the organization of the directional mechanisms within the receptive field. 3. When tested with single gratings, the directional tuning of 277 oriented cells in area 17 had a mean half width of 20.6 degrees, a mode near 13 degrees, and a range of 3.8-58 degrees. Simple cells were slightly more narrowly tuned than complex cells. The selectivity of LS neurons for the direction of moving gratings is not markedly different from that of neurons in area 17. The mean direction half width was 20.7 degrees. 4. We evaluated the directional selectivity of these neurons by comparing responses to stimuli moved in the optimal direction with those elicited by a stimulus moving in the opposite direction. In area 17 about two-thirds of the neurons responded less than half as well to the non-preferred direction as to the preferred direction; two-fifths of the units responded less than one-fifth as well. Complex cells showed a somewhat greater tendency to directional bias than simple cells. LS neurons tended to have stronger directional asymmetries in their response to moving gratings: 83% of LS neurons showed a significant directional asymmetry. 5. Neurons in both areas responded independently to each component of the plaid. Thus cells giving single-lobed directional-tuning curves to gratings showed bilobed plaid tuning curves, with each lobe corresponding to movement in an effective direction by one of the two component gratings within the plaid. The two best directions for the plaids were those at which one or other single grating would have produced an optimal response when presented alone.(ABSTRACT TRUNCATED AT 400 WORDS)     

Development of orientation tuning in simple cells of primary visual cortex

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.     

Region-specificity of GABAA receptor mediated effects on orientation and direction selectivity in cat visual cortical area 18

The role of GABAergic inhibition in orientation and direction selectivity has been investigated with the GABA_A-Blocker bicuculline in the cat visual cortex, and results indicated a region specific difference of functional contributions of GABAergic inhibition in areas 17 and 18. In area 17 inhibition appeared mainly involved in sculpturing orientation and direction tuning, while in area 18 inhibition seemed more closely associated with temporal receptive field properties. However, different types of stimuli were used to test areas 17 and 18 and further studies performed in area 17 suggested an important influence of the stimulus type (single light bars vs. moving gratings) on the evoked responses (transient vs. sustained) and inhibitory mechanisms (GABA_A vs. GABA_B) which in turn might be more decisive for the specific results than the cortical region. To insert the missing link in this chain of arguments it was necessary to study GABAergic inhibition in area 18 with moving light bars, which has not been done so far. Therefore, in the present study we investigated area 18 cells responding to oriented moving light bars with extracellular recordings and reversible microiontophoretic blockade of GABAergig inhibition with bicuculline methiodide. The majority of neurons was characterized by a pronounced orientation specificity and variable degrees of direction selectivity. GABA_Aergic inhibition significantly influenced preferred orientation and preferred direction in area 18. During the action of bicuculline orientation tuning width increased and orientation and direction selectivity indices decreased. Our results obtained in area 18 with moving bar stimuli, although in the proportion of affected cells similar to those described in area 17, quantitatively matched the findings for direction and orientation specificity obtained with moving gratings in area 18. Accordingly, stimulus type is not decisive in area 18 and the GABA_A dependent, inhibitory intracortical computations involved in orientation specificity are indeed region-specific and in comparison to area 17 less effective in area 18.     

Substructure of direction-selective receptive fields in macaque V1

We used two-dimensional (2-D) sparse noise to map simultaneous and sequential two-spot interactions in simple and complex direction-selective cells in macaque V1. Sequential-interaction maps for both simple and complex cells showed preferred-direction facilitation and null-direction suppression for same-contrast stimulus sequences and the reverse for inverting-contrast sequences, although the magnitudes of the interactions were weaker for the simple cells. Contrast-sign selectivity in complex cells indicates that direction-selective interactions in these cells must occur in antecedent simple cells or in simple-cell-like dendritic compartments. Our maps suggest that direction selectivity, and on and off segregation perpendicular to the orientation axis, can occur prior to receptive-field elongation along the orientation axis. 2-D interaction maps for some complex cells showed elongated alternating facilitatory and suppressive interactions as predicted if their inputs were orientation-selective simple cells. The negative interactions, however, were less elongated than the positive interactions, and there was an inflection at the origin in the positive interactions, so the interactions were chevron-shaped rather than band-like. Other complex cells showed only two round interaction regions, one negative and one positive. Several explanations for the map shapes are considered, including the possibility that directional interactions are generated directly from unoriented inputs.     

Correlations between directional and orientational tuning of cells in cat striate cortex

Summary Simple (N = 284) and complex cells (N = 125) in the central projection area (0–5° eccentricity) of the striate cortex of cats were stimulated with moving light bars and the responses to different directions of movement were recorded and plotted as polar-plots. Fourier analysis was applied to polar plots (SDO-analysis, Wörgötter and Eysel 1987; Wörgötter et al. 1990) to determine the general sensitivity (S) of the cells to visual stimulation, the directional (D) and orientational (O) tuning strength as well as preferred direction (PD) and preferred orientation (PO). Statistical distributions of the S, D and O parameters were determined for simple and complex cells of the cortical layers II–VI. Simple cells were more strongly tuned for direction and orientation than complex cells, whereas complex cells had a greater general sensitivity to visual stimulation. Directional tuning was significantly stronger in layer VI than in layer IV simple cells, otherwise no differences were detected between these two layers. We found that cells with large D and small O components are generally rare. The D and O components were plotted against each other to determine any possible correlation between the tuning strengths. The correlations were statistically significant for simple and complex cells but the correlation coefficients were very small (r < 0.3). It is suggested that only a very weak coupling between directional and orientational tuning exists, preferentially in the deeper layer simple cells.     

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.     

The role of GABAergic inhibition in the response properties of neurones in cat visual area 18

Bicuculline methiodide was iontophoretically applied to single neurones in cat area 18 to investigate how removal of gamma-aminobutyrate mediated inhibition affects the visual response properties. Moving sinusoidal gratings were used to study spatial and temporal response characteristics. Orientation sensitivity and spatial and temporal frequency tuning curves were determined with and without iontophoretically applied bicuculline. In most neurones, orientation sensitivity and spatial frequency tuning remained largely unaffected, whereas temporal frequency tuning was very much broadened. It is suggested that the dominant excitatory input to area 18 cells is a spatially organized input from area 17 and local inhibition in area 18 sharpens primarily temporal selectivity. An alternative explanation of our results would be that the distribution of synapses mediating temporal tuning in area 18 is fundamentally different from that mediating spatial frequency and orientation tuning, which may be located at sites distant from the cell body and relatively inaccessible to the drug application.     

The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat.

1. The iontophoretic application of the GABA antagonist bicuculline to simple and complex cells in the striate cortex of the cat produced extensive modifications of receptive field properties. These modifications appear to relate to a block or reduction of GABA-mediated intracortical inhibitory influences acting on the cells examined. 2. For simple cells the effects of bicuculline on receptive field properties involved a loss of the subdivision of the receptive field into antagonistic "on" and "off" regions, a reduction in orientation specificity and a reduction or elimination of directional specificity. 3. The effect on the "on" and "off" subdivisions of the simple cell receptive field was such that all stationary flashing stimuli, whether covering the whole receptive field, or located within the receptive field over a previously determined "on" or "off" region, resulted in an "on and off" response. 4. The orientation specificity of complex cells was reduced during the application of bicuculline such that in many cases the original specificity of the cell was virtually lost with the response to the orientation at 90 degrees to the optimal being of similar magnitude to the optimal. The directional specificity of complex cells was generally less affected than that of simple cells. Often when large changes in orientation specificity were observed the directional specificity was relatively unaffected. 5. For some cells apparently showing to all visual stimuli only inhibitory responses, the application of bicuculline resulted in the appearance of excitatory responses. 6. In all cases receptive field properties reverted to the original state after termination of the bicuculline application. It was not generally possible to duplicate the effects of bicuculline by raising neuronal excitability with iontophoretically applied glutamate. 7. On the basis of these results it is suggested that the normal subdivision of the simple cell receptive field into separate "on" and "off" regions and its directional specificity are dependent on intracortical inhibitory processes that are blocked by bicuculline. The orientational tuning of simple cells conversely appears to be largely determined by the excitatory input but normally enhanced by lateral type inhibitory processes acting in the orientation domain. 8. It also appears that the excitatory input to some complex cells is not orientation specific. This suggests that for these cells it is extremely unlikely that they receive an orientation specific excitatory input from simple cells.     

Responses to directional stimuli in retinal preganglionic units

1. Extracellular recordings were made from directionally selective ganglion cell units in the isolated frog retina and decapitated Necturus preparation.2. Intracellular recordings were made from individual photoreceptor cells in the frog and Necturus retinae while stimuli which had evoked directionally selective responses at the ganglion cell level were presented. No evidence for inhibition of photoreceptors for any direction of movement of the light stimulus was found. This appeared to rule out a mechanism for directional selectivity involving inhibition of photoreceptor potentials.3. Intracellular recordings were made from the nuclear layer between photoreceptors and ganglion cells in Necturus. The responses were of two types: either transitory or sustained.4. The sustained type responses could be divided into two classes depending on their receptive field organization. One type of sustained potential had a large receptive field without any evidence for a centre-surround antagonism and corresponded to the luminosity type S-potential recorded in fish. The other type had a smaller receptive field and showed a difference in sign of response between centre and surround if the centre was flooded with a steady light. This is very similar to what has been described for a type of on-centre, off-surround ganglion cell.5. The transitory type of responses showed some centre-surround antagonistic organization. Some of these transitory units also appeared to show some discrimination in response as a function of the distribution of light on the retina.6. No specific directional selectivity was found from units at the inner nuclear layer. This further excluded any mechanism of directional sensitivity which involves selectivity at the photoreceptor level.7. It was concluded that although inner nuclear layer units may play a role in the mechanism of directional selectivity, no specific directionality was found at the first synaptic level of the retina.