Single cells were recorded from cortical area V4 of two rhesus monkeys (Macaca mulatta) trained on a visual discrimination task with two levels of difficulty. Behavioral evidence indicated that the monkeys' discriminative abilities improved when the task was made more difficult. Correspondingly, neuronal responses to stimuli became larger and more selective in the difficult task. A control experiment demonstrated that changes in general arousal could not account for the effects of task difficulty on neuronal responses. It is concluded that increasing the amount of attention directed toward a stimulus can enhance the responsiveness and selectivity of the neurons that process it.

We seek a general approach to determine what stimulus features visual neurons are sensitive to and how those features are represented by the neuron's responses. Because lesions of inferior temporal (IT) cortex interfere with a monkey's ability to perform pattern discrimination tasks we studied IT neurons. Previous single-unit studies have shown that IT neurons sometimes respond more strongly to complex stimuli (brushes, hands, faces) than to simple stimuli (bars, slits, edges). However, it is not known how specific stimulus parameters are represented by responses. We studied the responses of IT neurons in alert behaving monkeys to a large set of two-dimensional black and white patterns. The stimulus set was based on 64 Walsh functions that can be used to represent any picture with a resolution of one part in eight along each of two dimensions. The responses to these stimuli spanned a continuum from inhibition to strong excitation. A statistical test showed that the spike count was determined by which Walsh stimulus was presented. Hence, these stimuli form an adequate set for testing IT neurons. The responses showed temporal modulation of the spike train that could not be represented by a change in the spike count alone. Examples of this modulation were changes in latency, changes in the duration of the response, and alternating periods of excitation and inhibition. This temporal modulation may be important in representing stimulus parameters. The next paper in this series develops a method for quantifying this temporal modulation and shows that it is dependent on the stimulus. The third paper in this series shows that this temporal modulation contains more information about stimulus parameters than is contained in the spike count alone.

1. 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. 2. 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. 3. 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. 4. 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.(ABSTRACT TRUNCATED AT 400 WORDS)

The time course of the response of a single cortical neuron to counterphase-grating stimulation may vary as a function of stimulation parameters, as shown in the preceding paper (19). The poststimulus-time histograms of the response amplitudes against time are single or double peaked, and where double peaked, the two peaks are of equal or unequal amplitudes. Furthermore, the spatial-phase dependence of cortical complex-cell responses may be a function of spatial frequency, so that the receptive field appears to have linear spatial summation at some spatial frequencies and nonlinear spatial summation at others (19). In the first part of this paper, we analyze a model receptive field that displays this behavior, and in the second part experimental data are presented and analyzed with regard to the model. The model cortical receptive field in its simplest form contains (two rows) of geniculate X-cell-like, DOG (difference-of-Gaussians)-shaped, center-surround antagonistic, circular-input subunits. We propose nonlinear summation between these two subunits, by introducing a half-wave rectification stage before pooling. The model is tested for the responses it predicts for the application of counterphase-grating stimulation. This simple model predicts the appearance of three response forms as a function of counterphase-stimulation parameters. At periodic spatial frequencies the expected-response histogram has a single peak, whose amplitude has a sinusoidal dependence on spatial phase. At spatial frequencies halfway between these, the expected-response histogram has two equal peaks whose amplitudes have a full-wave rectified sinusoidal dependence on spatial phase. At all intermediate spatial frequencies the expected-response histogram has a "mixed" form; the histogram appears sometimes with one peak, sometimes with two equal peaks, and generally with two peaks of unequal amplitude, as a function of spatial phase. Null responses are expected to appear at specific spatial phases only for the periodic spatial frequencies that give "pure" response time courses as in paragraph 5 above, and not in the more common mixed response case of paragraph 6. The analysis procedure described in the preceding paper (19) is used, separating the odd and even Fourier components of the response histograms reflecting the receptive-field intrasubunit linear summation and intersubunit nonlinear summation, respectively. We propose that this model may be used as a working hypothesis for the analysis of these aspects of the various cortical receptive-field types. Experimental data are described and discussed in terms of the model.(ABSTRACT TRUNCATED AT 400 WORDS)

To study the influence of task difficulty on the stimulus-elicited responses of inferior temporal (IT) neurons, the stimulus-elicited responses of 64 neurons were recorded from IT cortex of three rhesus monkeys while they performed three behavioral tasks-an irrelevant-stimulus task, a stimulus detection task, and a stimulus discrimination task. The monkey could ignore the stimulus entirely in the irrelevant-stimulus task, was required only to detect stimulus dimming in the stimulus detection task, and was required to attend to specific properties of the stimulus in the discrimination task. The excitatory responses in the discrimination and stimulus detection tasks were larger than those in the irrelevant-stimulus task (61% and 33%, respectively, of the individual differences were significant), and excitatory responses in the discrimination task were larger than those in the detection task (49% of the individual differences reached significance). Twenty percent of the stimulus presentations elicited inhibitory responses that were followed by off-responses. The off-responses were modulated by the tasks in the same order as the excitatory on-responses. Assuming that the off-response strengths indicate the depth of the stimulus-induced inhibition, these results suggest that inhibitory responses were influenced across these tasks in a manner similar to the excitatory responses. When the neuronal responses were related to the difficulties of these tasks, both the response strength and errors were seen to be least during the irrelevant-stimulus task and greatest during the discrimination task. This relationship suggests that the visual responsiveness of IT neurons is related to the degree of attention the animal pays to the stimulus.(ABSTRACT TRUNCATED AT 250 WORDS)