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

Abstract

Nested hippocampal oscillations in the rodent gives rise to temporal coding that may underlie learning, memory, and decision making. Theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples during quiescence. Whether these oscillatory regimes extend to primates is less clear. We therefore sought to identify correspondences in frequency bands, nesting, and behavioral coupling taken from macaque hippocampus. We found that, in contrast to the rodent, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. Beta/gamma (15-70Hz) had greater power during visual search while theta (7-10 Hz) dominated during quiescence. Moreover, delta/theta (3-8 Hz) amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, though the low frequencies coupled with higher, ripple frequencies (60-150 Hz). The distribution of spike-field coherence revealed three peaks matching the 3-10 Hz, 20-30 Hz and 60-150 Hz bands; however, the low frequency effects were primarily due to 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. These findings diverge from the rodent oscillatory canon and call for a shift in focus and frequency when considering the primate hippocampus.

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

“…To beter understand oscillatory composi�on 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 permuta�on test, Figure 2A), in line with previous studies [36][37][38] . Furthermore, the pyramidal layer showed rela�ve 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).…”

“…In this study, we sought to forge a link between the extensive understanding of CA1 microcircuit func�on from rats and mice 64,65 to the network dynamics and brain-behavior states seen during naturalis�c experiences in primates 36,37,42,66,67 . Building on previous work 58,59,68 , the semi-supervised clustering of waveforms and ISI distribu�ons of isolated CA1 single units iden�fied func�onal cell groups with diverse physiological characteris�cs.…”

“…Although many aspects of hippocampal physiology are conserved between rodents and primates, differences in oscillatory dynamics [36][37][38][39][40][41] and behavior-specific modula�on [42][43][44][45][46][47][48][49][50][51] suggest there may be phylogene�c specializa�ons that may be uncovered by an understanding of the underlying func�onal cell composi�on. A first-pass bisec�on of hippocampal (and medial temporal lobe) cells in primates into puta�ve inhibitory and excitatory classes (or four groups 52 ) reveals characteris�c responses at both the circuit-level 38,[52][53][54] and cogni�ve/behavioral levels 55,56 .…”

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)(5)(6)(7)(8)(9)(10)(11)(12) 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, 2021;Abbaspoor et al, 2022). 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).…”

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, 2021;Abbaspoor et al, 2022). 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).…”