Human single-neuron responses at the threshold of conscious recognition

Abstract

We studied the responses of single neurons in the human medial temporal lobe while subjects viewed familiar faces, animals, and landmarks. By progressively shortening the duration of stimulus presentation, coupled with backward masking, we show two striking properties of these neurons. (i) Their responses are not statistically different for the 33-ms, 66-ms, and 132-ms stimulus durations, and only for the 264-ms presentations there is a significantly higher firing. (ii) These responses follow conscious perception, as indicated by the subjects' recognition report. Remarkably, when recognized, a single snapshot as brief as 33 ms was sufficient to trigger strong single-unit responses far outlasting stimulus presentation. These results suggest that neurons in the medial temporal lobe can reflect conscious recognition by ''all-or-none'' responses.consciousness ͉ memory ͉ visual perception ͉ medial temporal lobe ͉ epilepsy O ur brain has the remarkable ability of creating coherent percepts despite constant changes in the visual environment. For example, our perception of a face is similar whether we see it for a fraction of a second or for much longer periods of time. Critically, below a certain temporal threshold, recognition appears to fail in an ''all-or-none'' fashion. Previous studies have addressed this question by using functional magnetic resonance imaging (fMRI) in humans (1). However, how our visual system represents this temporal nonlinearity at the single-neuron level is still an open question, because the fMRI signal gives only an indirect and temporally sluggish measure of the activity of large neural populations.Visual perception is processed along the ventral visual pathway, going from neurons in early visual areas extracting local visual features, to neurons in higher areas involved in the encoding and recognition of the actual object that is being seen (2-6). This processing culminates in the medial temporal lobe (MTL), which receives massive inputs from high-level visual areas. Converging evidence has shown that the MTL is not part of the recognition process per se (but see ref. 7), and it rather mediates the transformation of percepts into memories (8, 9). However, given their function in long-term memory storage, MTL neurons can indirectly ''signal'' perception processes because percepts should be represented in MTL if they are going to be stored in long-term memory for later recall. In particular, we recently reported the presence of neurons in the human MTL that fired selectively to different views of specific individuals, and in some cases even to their written name (10), thus showing the existence of an abstract representation that is invariant to basic visual features.To study the relationship of these MTL neurons to stimulus duration and how this correlates to conscious recognition, in the current study, we used different durations of stimulus presentations immediately followed by a mask. Stimulus durations were chosen to be at the threshold of recognition, so that the same visual stimulus c...

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