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.

Fig. 1.

Raster plots and peristimulus time histograms (PSTH) (100-ms bin size) of a single neuron in the right hippocampus that responded selectively to a picture of the patient's brother. Pictures are covered for privacy. The different presentation durations are shown with the light red bars at the bottom of the PSTH plots. Trials where the pictures were (were not) recognized are displayed in blue (red). Note that responses changed dramatically depending on whether the picture was recognized or not and far outlasted the stimulus presentation duration.

Fig. 2.

Raster plots and PSTH of a single neuron in the right entorhinal cortex that fired selectively to pictures of the World Trade Center. Note the striking difference in the responses to presentations when the picture was recognized (in blue) and when it was not (in red).

Fig. 3.

Raster plots and PSTH of a single neuron in the right hippocampus that responded selectively to pictures of the actress Whoopi Goldberg. In this case the patient reported to recognize all picture presentations of Whoopi Goldberg (in blue), even for the 33-ms presentations.

Fig. 4.

Raster plots and PSTH of a single unit in the left hippocampus that responded to a picture of Elvis Presley and a picture of Ronald Reagan. Note again the lack of responses in the nonrecognized trials.

Fig. 5.

Normalized average responses of all neurons for the different presentation durations, separated into recognized and nonrecognized trials. The horizontal dashed lines mark the mean baseline activity, and the bands show the SEM. Three effects can be seen. (i) a striking difference in amplitude and variability between recognized and nonrecognized conditions. (ii) A far longer neuronal response than stimulus presentation duration. (iii) A largely “unitary” response shape with only marginal changes with stimulus durations.

Fig. 6.

Normalized average responses of the cases in which the same duration elicited equal number of recognized and nonrecognized trials. The horizontal dashed lines mark the mean baseline activity and the bands show the SEM. Note that for the same stimulus and the same duration, i.e., exactly the same visual inputs, there was a significantly higher response for the trials in which the pictures were recognized, according to the subjects' reports (T test, P < 10⁻⁶).