1 Nature 2006 Vol: 442(7103):692-695. DOI: 10.1038/nature04982

Microstimulation of inferotemporal cortex influences face categorization

The inferior temporal cortex (IT) of primates is thought to be the final visual area in the ventral stream of cortical areas responsible for object recognition1, 2. Consistent with this hypothesis, single IT neurons respond selectively to highly complex visual stimuli such as faces3, 4, 5, 6. However, a direct causal link between the activity of face-selective neurons and face perception has not been demonstrated. In the present study of macaque monkeys, we artificially activated small clusters of IT neurons by means of electrical microstimulation while the monkeys performed a categorization task, judging whether noisy visual images belonged to 'face' or 'non-face' categories. Here we show that microstimulation of face-selective sites, but not other sites, strongly biased the monkeys' decisions towards the face category. The magnitude of the effect depended upon the degree of face selectivity of the stimulation site, the size of the stimulated cluster of face-selective neurons, and the exact timing of microstimulation. Our results establish a causal relationship between the activity of face-selective neurons and face perception.

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Figures
Figure 1: Visual stimuli and event timing.In each experimental session, the neural stimulus selectivity of several neighbouring cortical sites was first determined in a fixation task using luminance-matched face and non-face greyscale images. Then, in the second part of the experiment (a), face and non-face images with varying amounts of noise were used in a face categorization task. b, Timing of events in each categorization trial. One of the four possible microstimulation conditions shown was applied randomly in each trial. Figure 2: Effect of microstimulation of two representative face-selective neural clusters in IT cortex.a, Monkey KH; b, monkey FR. Data points show the proportion of face choices for different levels of visual signal in the images for different microstimulation conditions. The curves are logistic regression fits to the data points. The insets show averaged multiunit responses of the corresponding stimulated sites and their neighbouring sites. The inset abscissa shows the cortical position of the electrode tip along the recording track relative to the stimulated site (zero on the abscissa). The inset ordinate shows the averaged multi-unit neural responses. Responses to face and non-face stimuli are represented by red and blue bars, respectively. Colours are highlighted for the stimulated site. Error bars, s.e.m. Figure 3: Correlation between face selectivity of stimulated sites and the behavioural impact of microstimulation.a, Positive values on the y-axis represent psychometric function shifts in favour of face choices. Large d' values indicate higher selectivity for faces. Red data points indicate statistically significant shifts of the psychometric function. The correlation is significant for microstimulation at 50–100 ms and 100–150 ms conditions, but not for 0–50 ms (see text for details). b, Histogram of multiunit neural responses (smoothed with a 20-ms sliding window) to face (red line) and non-face (blue line) stimuli averaged from all stimulated face-selective (d' > 1) sites. Different microstimulation time windows are depicted by vertical lines. Figure 4: Effect of stimulus selectivity of neighbouring cortical sites on microstimulation results.Averaged shift in the psychometric function for the three stimulation conditions is shown for all stimulated face-selective (a) and non-selective (b) sites. Face-selective and non-selective sites were defined by d' > 1 and d' 1, respectively. Black columns represent sites with face-selective neighbours in their vicinity ( 500 m), and grey columns show sites with non-selective neighbour(s). Positive numbers on the y-axis show shifts in favour of face choices. Error bars, s.e.m.
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References
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    • . . . The inferior temporal cortex (IT) of primates is thought to be the final visual area in the ventral stream of cortical areas responsible for object recognition1, 2 . . .
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    • . . . Consistent with this hypothesis, single IT neurons respond selectively to highly complex visual stimuli such as faces3, 4, 5, 6 . . .
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    • . . . The degree of selectivity of each cortical site for face versus non-face images was measured by the d' index29, based on the following formula: . . .
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    • . . . where x is the visual signal and P(x) is the probability of face response, I1, I2 and I3 indicate the presence or absence of microstimulation in the three periods (one for stimulation present and zero for stimulation absent condition), and , and are free parameters (with 1 to 3 indicating the three stimulation conditions respectively) that were fitted using the maximum likelihood fitting procedure30 . . .
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