TEMPORAL ENCODING OF 2-DIMENSIONAL PATTERNS BY SINGLE UNITS IN PRIMATE PRIMARY VISUAL-CORTEX .1. STIMULUS-RESPONSE RELATIONS

Previously we developed a new approach for investigating visual system neuronal activity in which single neurons are considered to be communication channels transmitting stimulus-dependent codes in their responses. Application of this approach to the stimulus-response relations of inferior temporal (IT) neurons showed that these carry stimulus-dependent information in the temporal modulation as well as in the strength of their responses. IT cortex is a late station in the visual processing stream. Presumably the neuronal properties arise from the properties of the inputs. However, the discovery that IT neuronal spike trains transmit information in stimulus-dependent temporally modulated codes could not be assumed to be true for those earlier stations, so the techniques used in the earlier study were applied to single-striate cortical neurons in the studies reported here. Single-striate cortical neurons were recorded from three awake, fixating rhesus monkeys. The neurons were stimulated by two sets of patterns. The first set was made up of 128 black-and-white patterns based on a complete, orthogonal set of two-dimensional Walsh-Hadamard functions. These stimuli appear as combinations of black-and-white rectangles and squares, and they fully span the range of all possible black-and-white pictures that can be constructed in an 8 x 8 grid. Except for the stimulus that appeared as an all-white or all-black square, each stimulus had equal areas of white and black. The second stimulus set was made up of single bars constructed in the same 8 x 8 grid as the Walsh stimuli. These were presented both as black against a gray background and white against a gray background. The stimuli were centered on the receptive field, and each member of the stimulus set was presented once before any stimulus appeared again. The responses of 21 striate cortical neurons were recorded and analyzed. Two were identified as simple cells and the other 19 as complex cells according to the criteria originally used by Hubel and Wiesel. The stimulus set elicited a wide variety of response strengths and patterns from each neuron. The responses from both the bars and the Walsh set could be used to differentiate and classify simple and complex cells. The responses of both simple and complex cells showed striking stimulus-related strength and temporal modulation. For all of the complex cells there were instances where the responses to a stimulus and its contrast-reversed mate were substantially different in response strength or pattern, or both. Complex cells showed differential response modulation across the contrast sign of the stimulus to Walsh patterns or classical bar stimuli. The responses of most complex cells showed significant differences in their orientation tuning functions according to whether the tuning was determined with a light or dark bar on a gray background. These differences were even more striking when the temporal modulation was taken into account. These results suggest that complex cells are encoding multiple stimulus parameters such as pattern and contrast differentially in different aspects of the temporally modulated response.