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Phase Organization of Network Computations Available online at www.sciencedirect.com ScienceDirect Phase organization of network computations 1 1,2 Matthew A Wilson, Carmen Varela and Miguel Remondes Coupled oscillations are hypothesized to organize the cycle asymmetry [6], non-uniform distributions of processing of information across distributed brain circuits. This spike–LFP phase relationships, such as phase-locking idea is supported by recent evidence, and newly developed and precession [7], and theta-cycle skipping [8], suggest techniques promise to put such theoretical framework to that distinct phases of a cycle have their own function in mechanistic testing. We review evidence suggesting that information processing. On the basis of these observa- individual oscillatory cycles constitute a functional unit that tions, the phase of oscillations has been hypothesized to organizes activity in neural networks, and that oscillatory phase be a temporal organizer of neural activity, one that allows (defined as the fraction of the wave cycle that has elapsed the processing and transferring of information within and relative to the start of the cycle) is a key oscillatory parameter to between brain circuits. implement the functions of oscillations in limbic networks. We highlight neural manipulation techniques that currently allow for The oscillatory cycle as a functional unit causal testing of these hypotheses. As animals explore an environment, a subset of hippocam- Addresses pal neurons display increased firing rates when the animal The Picower Institute for Learning and Memory, Department of Brain and occupies restricted spatial locations of the environment. Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Therefore, ensembles of these cells afford a place-code MA, USA based on neuronal firing rate [9]. The rate code is suffi- Corresponding author: Wilson, Matthew A ([email protected]) ciently robust to allow us to predict the animal’s location at any given time [10]. What then, is the role of phase in hippocampal place coding? As the animal traverses a given Current Opinion in Neurobiology 2015, 31:250–253 neuron’s receptive field, the phase corresponding to indi- vidual spikes changes in consecutive cycles of the theta This review comes from a themed issue on Brain rhythms and dynamic coordination oscillation (4–12 Hz, 10 cycles per place-field), with spikes advancing progressively towards the peak of the Edited by Gyo¨ rgy Buzsa´ ki and Walter Freeman theta cycle, a phenomenon called theta phase-precession For a complete overview see the Issue and the Editorial [7]. As illustrated in Figure 1, theta phase-precession allows Available online 11th February 2015 a more precise encoding of location, providing a measure of http://dx.doi.org/10.1016/j.conb.2014.12.011 the distance that the animal has travelled within the 0959-4388/# 2015 Elsevier Ltd. All rights reserved. receptive field; importantly, it also means that different spatial information is encoded at different phases. This phase asymmetry has an additional consequence at the population level (Figure 1): within a single theta cycle, spikes from place cells with overlapping fields represent where the animal was, where it is, and where it will be in the Introduction form of so-called theta sequences [11,12]. This suggests Oscillatory activity has been associated with the encod- that the single theta cycle is a functional unit capable of ing, communication, and storage of information in ner- representing distinct temporal–spatial content at different vous systems. As such, distinct oscillatory frequencies are phases. correlated with distinct behavioral states. In the hippo- campus, theta oscillations are observed during explora- In addition to the segregation of information at different tion, while ripple oscillations, which coincide with phases within a cycle, there is also distinct processing across population firing patterns that may represent the activa- successive oscillatory cycles. In the medial entorhinal tion of memory traces, occur during sleep and awake cortex (mEC), spikes from neurons selective for the animal immobility [1,2]. In neocortex, gamma oscillations have head-direction skip every other theta cycle when they fire been associated with attention [3], and working memory in their preferred phases, while they fire in every cycle [4], while alpha and beta bands may orchestrate the when in non-preferred phases. In other words, different representation and selection of rules [5]. While we can cycles segregate at least two populations of neurons with indeed draw a correspondence between oscillatory fre- distinct head-directionality [8]. Thus, in addition to phase- quency and behavior, phenomena such as oscillatory specific processing, head-direction neurons exhibit a 1 These authors contributed equally to this work. 2 Present address: Instituto de Medicina Molecular, Faculdade de Medicina da Universidade de Lisboa, Portugal. Current Opinion in Neurobiology 2015, 31:250–253 www.sciencedirect.com Phase organization of network computations Wilson, Varela and Remondes 251 Figure 1 Current Time/Position Place Fields ABC Cell 1 Cell 2 Cell 3 Cell 4 Cell 5 LFP ∼125ms PHASE PRECESSION THETA SEQUENCE A B C Past Current Future Location Location Location Current Opinion in Neurobiology Oscillatory cycles and phase organize place cell activity in hippocampus. The overlapping place fields of five principal cells are represented schematically and color-coded. The corresponding vertical bars represent the spikes from each place cell as the animal traverses the receptive fields from left to right. Below is the raw local field potential (LFP), overlaid with the same signal filtered in the theta band (4–12 Hz, black), to illustrate the theta rhythm that dominates during locomotion and exploration. As the animal moves across each place field, the spikes of that cell occur at progressively earlier phases of the hippocampal theta rhythm (phase precession; e.g. green spikes). As a consequence, for any given theta cycle, the spikes of place fields extending behind (‘A’) and ahead (‘C’) of the animal occur at different phases, effectively generating a compressed representation of a spatial trajectory (theta sequence, spikes in ‘ABC’). Note that, without the phase information, the position within a receptive field could not be estimated from the spikes of that cell alone; also, without theta sequences, the representation of the same spatial trajectory would require computation over several cycles. cycle-specific processing, one that segregates information happened, the segregation of representations occurred between consecutive cycles and might contribute to com- chiefly during the second half of the theta cycle [14], putations that span multiple theta cycles. Pharmacological reflecting phase specific contextual segregation, possibly disruption of this functional cycle-offset was found to to preserve the integrity of both representations and en- suppress the unique grid-shaped place selectivity of hance the discriminative power between environments. mEC neurons, suggesting a functional role in space repre- These results indicate the ability for the theta oscillation sentation [8]. Cycle skipping has been observed in other to segregate information sources at distinct within-cycle areas of the entorhinal cortex (reviewed by Brandon et al.), phases and also across cycles, potentially contributing to and elsewhere in the limbic system, namely in neurons from longer computations. the thalamic nucleus reuniens, and specifically in those that were not involved in head-direction coding, suggesting its If information is indeed segregated by oscillatory phases contribution to the processing of other types of information and cycles, accessing this information by distant brain [13]. Cycle-specific processing is also demonstrated in areas requires cycle and phase-specific coordinated activ- hippocampal CA3 place-selective populations, whose ac- ity, or phase-coherence [15]. Instances suggesting that tivity can represent different contexts by spontaneously one brain region can ‘read’ the contents encoded in switching back and forth between two contextual repre- another, through oscillatory coherence, have been broadly sentations in consecutive theta cycles. Although mixed reported; namely, during multi-feature representation representations within a cycle were rare, when they [16,17], and sensory information integration [18]. Coherent www.sciencedirect.com Current Opinion in Neurobiology 2015, 31:250–253 252 Brain rhythms and dynamic coordination neural activity has been reported between multiple brain when animals are close to choice points in a multi-choice areas and the hippocampus at the theta frequency, which is task, and the amount of choice-relevant information a timescale that is relevant for plasticity,memory formation, processed increases [35]. Spikes that initially are essen- and decision-making [19–24]. The phase-coordinated acti- tially simultaneous, develop a hippocampus-cingulate vation of these regions has been suggested to contribute to a delay of about 80 ms. Such timing relation might serve, variety of task-related functions, such as working memory, or even represent, the integration and processing of reward prediction, and decision-making [20,25–27]. incoming hippocampal information by cingulate neuronal populations, something seen in previous studies relating Recently reported interactions between hippocampal CA3, hippocampus and entorhinal cortex [39]. CA1, and mEC suggest that oscillatory phase could indeed
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