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Differences in the emergent coding properties of cortical and striatal ensembles

Abstract

The function of a given brain region is often defined by the coding properties of its individual neurons, yet how this information is combined at the ensemble level is an equally important consideration. We recorded multiple neurons from the anterior cingulate cortex (ACC) and the dorsal striatum (DS) simultaneously as rats performed different sequences of the same three actions. Sequence and lever decoding was markedly similar on a per-neuron basis in the two regions. At the ensemble level, sequence-specific representations in the DS appeared synchronously, but transiently, along with the representation of lever location, whereas these two streams of information appeared independently and asynchronously in the ACC. As a result, the ACC achieved superior ensemble decoding accuracy overall. Thus, the manner in which information was combined across neurons in an ensemble determined the functional separation of the ACC and DS on this task.

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Figure 1: Behavior was similar for common segment lever presses in different sequence blocks.
Figure 2: No regional differences in the way individual neurons responded to presses in different sequence blocks or on different physical levers.
Figure 3: Comparison of the signal detection characteristics of single neurons versus ensembles.
Figure 4: Sequence information is represented as differences in ensemble activity state patterns in both the ACC and DS.
Figure 5: Consistency of sequence encoding in the ACC and DS within behavioral epochs.
Figure 6: Comparison of the timing of maximal sequence and lever differentiation in ACC and DS ensembles.

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Acknowledgements

This research was supported by Canadian Institutes of Health Research grants (MOP-93784 and MOP-84319).

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Authors

Contributions

J.K.S. and L.M. designed the study, L.M. conducted the experiments, L.M., J.M.H., A.J.L. and J.K.S. performed data analysis and created the figures, A.G.P. helped interpret the results and write the manuscript.

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Correspondence to Liya Ma.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Task description and performance.

a) The operant chamber contained 3 levers installed on the front panel and a food-cup on the opposing wall. A unique sensory cue was attached to the floor immediately in front of each lever as well as on the surrounding wall. The 1st lever (light gray in schematic) to be pressed in a given sequence block could have Velcro attached, the 2nd lever (dark gray in schematic) cardboard attached and the 3rd lever (black in schematic), soft foam attached. b) Example of a typical test day where the rat had to perform a minimum of 10 trials on each of the 3 sequence blocks, which were given in a pseudorandom order. On this session, sequence block A required the rat to respond on the right lever, followed by the middle lever and then the left lever, before reward pellets were delivered to the food-cup on the opposite wall. The serial order of the 3 sensory cues (velcro, cardboard, foam) remained constant for a given rat but were moved to different levers for each of the sequence blocks.

Supplementary Figure 2 Histology showing recording sites.

a) Histology showing representative electrode track endings (white arrows) in the ACC. b) Schematics showing the location and range of the recording sites in the ACC. Given that not all electrodes left a track, the recording range was inferred based on the visible tracks and the size of the electrode arrays. c) Representative electrode track endings (white arrows) in the DS. d) Schematics showing the location and range of the recording sites in the DS.

Supplementary Figure 3 Firing properties in the ACC and DS.

The iFRs from all bins and neurons were combined for each region, and their probability density functions were plotted on a logarithmic scale. Although both ACC and DS neurons usually have low firing rates, DS neurons exhibited brief periods of high activity more often than did ACC neurons, giving rise to the long-tailed firing rate distribution (DS: gray, ACC: black).

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Ma, L., Hyman, J., Lindsay, A. et al. Differences in the emergent coding properties of cortical and striatal ensembles. Nat Neurosci 17, 1100–1106 (2014). https://doi.org/10.1038/nn.3753

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