Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Chained Activation of Neuronal Assemblies supports Major Cognitive Processes


Science  16 Sep 2016: Vol. 353, Issue 6305, pp. 1280-1283

Awake hippocampal reactivations project onto orthogonal neuronal assemblies

Arnaud Malvache,

INMED, INSERM U901, Aix-Marseille Université, Marseille, France.


The chained activation of neuronal assemblies is thought to support major cognitive processes, including memory. In the hippocampus, this is observed during population bursts often associated with sharp-wave ripples, in the form of an ordered reactivation of neurons. However, the organization and lifetime of these assemblies remain unknown. We used calcium imaging to map patterns of synchronous neuronal activation in the CA1 region of awake mice during runs on a treadmill. The patterns were composed of the recurring activation of anatomically intermingled, but functionally orthogonal, assemblies. These assemblies reactivated    discrete temporal segments of neuronal sequences observed during runs and could be stable across consecutive days. A binding of these assemblies into longer chains revealed temporally ordered replay. These modules may represent the default building blocks for encoding or retrieving experience.

The concept of “cell assembly” refers to a group of neurons that are coactivated repeatedly for a given brain operation. Cell assemblies thus represent a distinct cognitive entity embedded within neuronal networks. However, both their basic structural and functional organization, when outside world influences are minimal, as well as their long-term dynamics, remain unknown owing to the experimental difficulty of circumscribing them. In principle, the chained coordinated activation of such neuronal assemblies combines into sequences of neuronal activation supporting complex cognitive processes. Therefore, sequences of neuronal activation can represent a remarkable motif for revealing the activation of underlying neuronal assemblies. In the hippocampus,    sequences occur at multiple time scales in the CA1 region—e.g., at the time frame of behavior—or compressed within the period of fast network oscillations. They can integrate time and/or distance, as well as any contextual information. Of particular interest are the coordinated patterns of neuronal activation that occur during awake immobility and that are related to sharp wave–associated ripples (SWRs), because these are produced when bodily or environmental control over hippocampal dynamics is minimal. Even though these coherent population events include sequential place cell reactivation representing past or future spatial experience, they are indeed also critically shaped by the internal functional organization of local circuits. Sequential neuronal reactivation can be split into separate chunks of current or remote experience, but their spatiotemporal organization into different cell assemblies remains unknown. So far, the dissection of hippocampal sequences into discrete reactivation patterns has been achieved by mapping them onto an external spatiotemporal template, such as an experienced behavior. It is important to minimize external sensory inputs to reveal the default organization of hippocampal dynamics into cell assemblies    because local inputs are known to bias the content of both local and remote replay. We recently described a paradigm for revealing internally driven spatiotemporal sequences that occur during run behavior, which is particularly well suited to address this issue.

However, monitoring large-scale multineuronal activity at high cellular density to identify cell assemblies    represents a major technical challenge. This is particularly critical in the case of hippocampal population bursts, as they involve local microcircuits within the densely packed pyramidal layer. In vivo imaging of hippocampal dynamics is ideally suited to circumvent this limitation.

We used chronic two-photon calcium imaging    of awake head-restrained mice allowed to self-regulate their motion in the dark on a nonmotorized treadmill.

This study sheds light on the basic organization of awake CA1 synchronous population bursts that include ripples. These events fall into three distinct categories. Most of them recruit neurons sampled among a finite repertoire of preconfigured cell assemblies; these are mutually exclusive and therefore mathematically “orthogonal.” Multiple-assembly SCEs preferentially bind these assemblies into the replay of ongoing internal dynamics on a compressed time scale, as reported for the extended replay phenomenon. This finding was enabled by the use of large-scale chronic calcium imaging combined with the mapping of ripples onto default recurring spatiotemporal sequences. Unfortunately, the temporal resolution of calcium imaging does not allow an exact determination of the time interval within which coactivation occurs for cells in the same assembly or across different assemblies. Multiple-assembly SCEs may indeed still bind together orthogonal assemblies, spreading across different gamma cycles. We hypothesize that orthogonal assemblies could be the calcium counterpart of the recently described attractors within trajectory replay, and that their combination would form the discontinuous representation of space in single awake ripples. The awake replay of memory-related information during SWRs has been shown to support encoding, consolidation, and retrieval of event memories and to guide memory-guided decision-making. The neuronal assemblies revealed here might indeed constitute separate attractor states, forming the building blocks onto which experience is encoded.

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