Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus

Abstract

Nested hippocampal oscillations in the rodent give rise to temporal dynamics that may underlie learning, memory, and decision making. Although theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples emerge in quiescence, it is less clear that these oscillatory regimes extend to primates. We therefore sought to identify correspondences in frequency bands, nesting, and behavioral coupling of oscillations taken from macaque hippocampus. We found that, in contrast to rodent oscillations, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. In both stationary and freely-moving designs, beta2/gamma (15-70 Hz) had greater power during visual search whereas the theta band (3-10 Hz; peak ~8 Hz) dominated during quiescence and early sleep. Moreover, theta band amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, instead occurring along with higher frequencies (60-150 Hz). Spike-field coherence was most frequently seen in these three bands, (3-10 Hz, 20-35 Hz and 60-150 Hz); however, the theta-band coherence was largely due to spurious coupling during sharp-wave ripples. Accordingly, no intrinsic theta spiking rhythmicity was apparent. These results support a role for beta2/slow gamma modulation in CA1 during active exploration in the primate that is decoupled from theta oscillations. The apparent difference to the rodent oscillatory canon calls for a shift in focus of frequency when considering the primate hippocampus.

Circuit dynamics of superficial and deep CA1 pyramidal cells and inhibitory cells in freely-moving macaques

“…To better understand oscillatory composition across layers, we computed aperiodic-corrected power spectra (Figure 2A). Despite inter-subject differences in absolute peak frequencies across the spectrum, both subjects showed reduced theta-band power (5-10 Hz) during the task in comparison to early sleep overnight, across all recorded channels (p<0.05, cluster-based permutation test, Figure 2A), in line with previous studies 36–38 . Furthermore, the pyramidal layer showed relative increases in power in the mid frequencies of 15-40 Hz (Figure 2A), and each animal had a preferred higher gamma band apparent during the task (Figure S2A).…”

“…their distribution in depth. Mesoscopic CA1-population/hippocampal spectrotemporal activity shows considerable differences in macaques relative to rats and mice 33,35,59–61 . For example, some aspects of gamma and sharp-wave ripples appear well conserved across species, whereas the multiple circuit mechanisms driving hippocampal theta-band oscillations in rats and mice have yet to be dissected in primates.…”

“…Although many aspects of hippocampal physiology are conserved between rodents and primates, differences in oscillatory dynamics [33][34][35][36][37][38] and behavior-specific modula�on [39][40][41][42][43][44] suggest there may be phylogene�c specializa�ons that an understanding of the underlying func�onal cell composi�on may uncover. A first-pass bisec�on of hippocampal (and medial temporal lobe) cells in primates into puta�ve inhibitory and excitatory classes (or four groups 45 ) reveals characteris�c responses at both the circuitlevel 35,46,47 and cogni�ve/behavioral levels 48,49 .…”

A dynamical computational model of theta generation in hippocampal circuits to study theta-gamma oscillations during neurostimulation

“…These conflicting results may originate from differences in experimental protocols and from a poor understanding of their biophysical underpinnings. Among such mechanisms, the involvement of hippocampal theta oscillations (4-12 Hz) and their interactions with higher-frequency gamma oscillations (30-120 Hz) in memory-related processes has been reported in multiple studies ( Lisman et al, 2005 ; de Almeida et al, 2007 ; Lega et al, 2012 ; Lin et al, 2017 ; Malkov et al, 2022 ; Abbaspoor et al, 2023 ). Moreover, the modulation of gamma oscillations by the phase of theta oscillations in hippocampal circuits, a phenomenon termed theta-gamma phase-amplitude coupling (PAC), correlates with the efficacy of memory encoding and retrieval ( Jensen and Colgin, 2007 ; Tort et al, 2009 ; Canolty and Knight, 2010 ; Axmacher et al, 2010 ; Fell and Axmacher, 2011 ; Lisman and Jensen, 2013 ; Lega et al, 2016 ).…”

Learning of object-in-context sequences in freely-moving macaques

“…More recently, some of the technological improvements for wireless recordings can free these restrictions and capitalize on the natural multisensory richness of stimuli-in-context (Mao et al, 2021; Schwarz et al, 2014; Berger et al, 2020; Voloh et al, 2023; Courellis et al, 2019; Stangl et al, 2023; Talakoub et al, 2019). offering more direct comparisons with neurophysiological studies in freely moving rats and mice (Abbaspoor et al, 2023). Furthermore, experiments in monkeys that use naturalistic behavioral contexts are more likely to translate to the conditions of human memory “in situ”, (Shamay-Tsoory and Mendelsohn, 2019).…”