An investigation of Hebbian phase sequences as assembly graphs

Abstract

Hebb proposed that synapses between neurons that fire synchronously are strengthened, forming cell assemblies and phase sequences. The former, on a shorter scale, are ensembles of synchronized cells that function transiently as a closed processing system; the latter, on a larger scale, correspond to the sequential activation of cell assemblies able to represent percepts and behaviors. Nowadays, the recording of large neuronal populations allows for the detection of multiple cell assemblies. Within Hebb's theory, the next logical step is the analysis of phase sequences. Here we detected phase sequences as consecutive assembly activation patterns, and then analyzed their graph attributes in relation to behavior. We investigated action potentials recorded from the adult rat hippocampus and neocortex before, during and after novel object exploration (experimental periods). Within assembly graphs, each assembly corresponded to a node, and each edge corresponded to the temporal sequence of consecutive node activations. The sum of all assembly activations was proportional to firing rates, but the activity of individual assemblies was not. Assembly repertoire was stable across experimental periods, suggesting that novel experience does not create new assemblies in the adult rat. Assembly graph attributes, on the other hand, varied significantly across behavioral states and experimental periods, and were separable enough to correctly classify experimental periods (Naïve Bayes classifier; maximum AUROCs ranging from 0.55 to 0.99) and behavioral states (waking, slow wave sleep, and rapid eye movement sleep; maximum AUROCs ranging from 0.64 to 0.98). Our findings agree with Hebb's view that assemblies correspond to primitive building blocks of representation, nearly unchanged in the adult, while phase sequences are labile across behavioral states and change after novel experience. The results are compatible with a role for phase sequences in behavior and cognition.

Coupled variability in primary sensory areas and the hippocampus during spontaneous activity

“…The stereotaxic coordinates for craniotomy and probe insertion in V1 combined information from Paxinos Atlas44 and recent studies30454647. The 64-channel silicon probe was then inserted around the central coordinate along the direction defined by the AP axis.…”

“…The data recorded from freely behaving animals have been extensively described in previous publications30454647. Thus, a brief description of the data is provided here.…”

Donald O. Hebb and the Organization of Behavior: 17 years in the writing

“…Although Orbach [146] claimed that the idea of the cell assembly originated with Lashley, Milner [136] refutes this in no uncertain terms. There are numerous other reviews of the cell assembly that indicate its importance in theories of brain function [4,41,97,122,144,147,187].…”

“…Finally, Hebb's concept of phase sequences as synchronized sets of cell assemblies has been examined by recording action potentials from the hippocampus and cortex of actively behaving rats [4]. The results suggest that the cell assemblies are the building blocks of neural representations, while the phase sequences that link cell assemblies are modifiable by new experiences, modulating the neural connections of cognition and behaviour.…”

“…While the Hebb synapse has become the most cited, and "better known than Donald Hebb himself" [166], the cell assembly may be his most lasting legacy [41,97,122,153,163]. Research on the phase sequence has lagged behind, but multi-electrode recording techniques have enabled researchers to investigate the integration of cell assemblies into larger phase sequences [4,129]. The Organization of Behavior remains influential because it continues to stimulate research in many areas of neuroscience including studies of learning and memory; the long-term effects of environment on development; aging; computer modeling of the brain, robotics, and artificial intelligence [21].…”