Abstract
Repeated viewing of an image over days and weeks induces a marked reduction in the strength with which neurons in monkey inferotemporal cortex respond to it. The processing advantage that attaches to this reduction is unknown. One possibility is that truncation of the response to a familiar image leaves neurons in a state of readiness to respond to ensuing images and thereby enhances their ability to track rapidly changing displays. We explored this possibility by assessing neuronal responses to familiar and novel images in rapid serial visual displays. Inferotemporal neurons responded more strongly to familiar than to novel images in such displays. The effect was stronger among putative inhibitory neurons than among putative excitatory neurons. A comparable effect occurred at the level of the scalp potential in humans. We conclude that long-term familiarization sharpens the response dynamics of neurons in both monkey and human extrastriate visual cortex.
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Acknowledgements
We thank K. McCracken for technical assistance. This work was supported by grants from the US National Institutes of Health (RO1 EY018620, P50 MH084053, K08 MH080329) and by the Pennsylvania Department of Health's Commonwealth Universal Research Enhancement Program. Technical support was funded by grants from the US National Institutes of Health (P30 EY08098 and P41RR03631).
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C.R.O. provided oversight and resources for the nonhuman primate study. T.M. and C.R.O. designed the experiment. T.M. trained the monkeys and collected the data. R.Y.C. provided oversight and resources for the human study. C.W. and R.Y.C. collected and analyzed the human data. All of the authors participated in the preparation of the manuscript.
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Integrated supplementary information
Supplementary Figure 1 Population activity of 29 neurons in Monkey 1
The difference between novel and familiar image strings with regard to the amplitude of driven periodic activity, as shown in (a), achieved statistical significance (p = 0.011, Mann-Whitney U-test, n = 29). The difference between novel and familiar image sequences with respect to the strength of the response to the trailing probe, as shown in (e-f), achieved statistical significance (p = 0.031, paired t-test on firing rate 100-200 ms following offset of the leading image, n = 29). Panels (a-b) observe the conventions of panels (a-b) in Fig. 2 and panels (c-f) observe the conventions of panels (a-d) in Fig. 5.
Supplementary Figure 2 Population activity of 37 neurons in Monkey 2
The difference between novel and familiar image strings with regard to the amplitude of driven periodic activity, as shown in (a), achieved statistical significance (p = 0.0013, Mann-Whitney U-test, n = 37). The difference between novel and familiar image sequences with respect to the strength of the response to the trailing probe, as shown in (e-f), achieved statistical significance (p = 0.000013, paired t-test on firing rate 100-200 ms following offset of the leading image, n = 37). Panels (a-b) observe the conventions of panels (a-b) in Fig. 2 and panels (c-f) observe the conventions of panels (a-d) in Fig. 5.
Supplementary Figure 3 Identical images elicit strong or weak periodic responses according to whether they are familiar or novel.
In six cases, we recorded from a neuron in monkey 1 and a neuron in monkey 2 using four images that were identical short of their training status. Two of the images were familiar to monkey 1 (set 1) and the other two were familiar to monkey 2 (set 2). Images familiar to monkey 1 elicited strong periodic activity in monkey 1 - red curve in (a) - and not in monkey 2 - red curve in (b). Images familiar to monkey 2 elicited strong periodic activity in monkey 2 - blue curve in (b) - and not in monkey 1 - blue curve in (a). Even in this small number of sessions, the difference between novel and familiar image strings with regard to the amplitude of driven periodic activity achieved significance (p = 0.031, Bootstrap test based on shuffling of novel and familiar trials).
Supplementary Figure 4 Neurons were distributed bimodally with respect to action potential width.
(a) Distribution across all 66 neurons of the interval in time between the maximal and minimal voltage attained by the average waveform during the millisecond following initiation. The best-fit Gaussian function is superimposed on each mode. Red and blue indicate neurons on the fast-spiking and regular-spiking sides of the cut in the distribution. (b) Average action-potential waveforms for all 66 neurons. Red and blue indicate waveforms classified as fast-spiking and regular-spiking. There is good within-category consistency with a single exception. (c) Fast-spiking neurons (red) tended to have a lower baseline firing rate than regular-spiking neurons (blue).
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Meyer, T., Walker, C., Cho, R. et al. Image familiarization sharpens response dynamics of neurons in inferotemporal cortex. Nat Neurosci 17, 1388–1394 (2014). https://doi.org/10.1038/nn.3794
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DOI: https://doi.org/10.1038/nn.3794
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