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Sharp emergence of feature-selective sustained activity along the dorsal visual pathway

Abstract

Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex.

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Figure 1: Anatomical location of recorded neurons.
Figure 2: Firing rate across task periods for example neurons in MT, MST and LPFC.
Figure 3: Direction discriminability in MT, MST and LPFC.
Figure 4: Direction decoding accuracy for the populations of MT, MST and LPFC neurons.
Figure 5: Relationship between task performance and delay-period direction discriminability of MST and LPFC neurons.
Figure 6: Choice probability of delay activity in MST and LPFC neurons.
Figure 7: Direction discriminability of LFP power in MT during working memory.
Figure 8: Spike-field synchrony between LPFC and MT during working memory.

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Acknowledgements

This study was supported by grants awarded to J.C.M.-T. from the Canadian Institutes of Health Research (CIHR), the Canada Research Chairs Program (CRC) and the EJLB Foundation. We thank M. Schneiderman for assistance with electrophysiological recordings, and W. Kucharski and S. Nuara for technical assistance.

Author information

Authors and Affiliations

Authors

Contributions

D.M.-H. and J.C.M.-T. designed the experiments. D.M.-H. and S.T. conducted the experiments. D.M.-H. analyzed the data. D.M.-H. and J.C.M.-T. wrote the article. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Julio C Martinez-Trujillo.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Receptive field sizes of MT and MST neurons.

Histogram showing the distribution of receptive field diameters (in degrees of visual field) for neurons recorded in MT (green) and MST (blue).

Supplementary Figure 2 Additional measures of percentage of selective neurons.

Percentage of selective neurons with sensory selectivity (upright solid bars), and delay selectivity (inverted hashed bars) in MT (green), MST (blue) and LPFC (red), measured separately for each of the two monkeys (a,b), and measured with a one-factor ANOVA testing a significant main effect of motion direction on mean firing rates across each task period (c). (d) Percentage of selective neurons with delay selectivity measured excluding the first 240 ms (light colors) or 480 ms (dark colors) of the delay.

Supplementary Figure 3 Distribution of duration of discriminability across the population of recorded neurons.

Cumulative histograms showing the percentage of selective neurons in MT (green), MST (blue) and LPFC (red) that exceeded each duration of discriminability during the sample (a,b) and the delay (c,d) periods, measured for each neuron as the percentage of bins with significant discriminability (a,c) or as the maximum percentage of consecutive significant bins (b,d).

Supplementary Figure 4 Time course of delay period choice probability.

Mean choice probability (± standard error) across delay-selective neurons in MST (a) and LPFC (b) over time during the delay period. Horizontal axis shows time after sample offset. Dashed line shows chance level of choice probability.

Supplementary Figure 5 Direction discriminability of LFP power in MST and LPFC during the delay period.

(a,b) For each frequency band, percentage of LFP sites in MST (a) and LPFC (b) for which the LFP power auROC in the delay period was significantly higher than expected by chance. (c,d) Mean auROC (± standard error) among selective sites in MST (c) and LPFC (d).

Supplementary Figure 6 Randomized surrogate spike-field synchrony between LPFC and MT during the delay period.

(a) Randomized surrogate phase coherence between LPFC spikes and MT LFPs during the delay period (computed from data with shuffled trial labels) as a function of LFP frequency for all significantly coherent LPFC-MT pairs, sorted in the same order as in Fig. 8b. (b) Percentage of coherent pairs for which the corresponding randomized surrogate coherence reached significance at each frequency. Frequency bands are color-coded.

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Mendoza-Halliday, D., Torres, S. & Martinez-Trujillo, J. Sharp emergence of feature-selective sustained activity along the dorsal visual pathway. Nat Neurosci 17, 1255–1262 (2014). https://doi.org/10.1038/nn.3785

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