Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

The hippocampus, including the dorsal dentate gyrus (dDG), and cortex engage in bidirectional communication. We propose that low-frequency activity in hippocampal-cortical pathways contributes to brain-wide resting-state connectivity to integrate sensory information. Using optogenetic stimulation and brain-wide fMRI and resting-state fMRI (rsfMRI), we determined the large-scale effects of spatiotemporal-specific downstream propagation of hippocampal activity. Low-frequency (1 Hz), but not high-frequency (40 Hz), stimulation of dDG excitatory neurons evoked robust cortical and subcortical brain-wide fMRI responses. More importantly, it enhanced interhemispheric rsfMRI connectivity in various cortices and hippocampus. Subsequent local field potential recordings revealed an increase in slow oscillations in dorsal hippocampus and visual cortex, interhemispheric visual cortical connectivity, and hippocampal-cortical connectivity. Meanwhile, pharmacological inactivation of dDG neurons decreased interhemispheric rsfMRI connectivity. Functionally, visually evoked fMRI responses in visual regions also increased during and after low-frequency dDG stimulation. Together, our results indicate that low-frequency activity robustly propagates in the dorsal hippocampal-cortical pathway, drives interhemispheric cortical rsfMRI connectivity, and mediates visual processing.hippocampus | resting-state functional connectivity | optogenetic | fMRI | low frequency T he hippocampus (HP) plays a prominent role in central nervous system functions, particularly in episodic memory (1, 2) and spatial navigation (3, 4). The HP, including the dentate gyrus (DG), can evoke large-scale influences on cortical activity, because the HP receives convergent information from sensory and limbic cortices before sending reciprocal divergent projections to create a highly interactive corticohippocampal-cortical network. The HP, including DG, CA3, and CA1, and neocortex, are connected via the entorhinal cortex (EC) (5, 6), such that the dorsolateral-to-ventromedial projection that originates in the EC corresponds to a dorsoventral axis of termination in the HP (5). This anatomical topography suggests that a functional gradient could exist along the HP dorsoventral axis. Previous studies demonstrated that dorsal HP (dHP) and cortex are functionally integrated during sensory processing and memory consolidation (7-9). Specifically, dHP can integrate multimodal sensory information and process memory operations (7) using excitatory longrange projections (10). This process occurs over multiple brain circuits, but the role of dHP in complex networks, particularly its influence on brain-wide functional connectivity, is not well understood.Resting-state functional MRI (rsfMRI) (11-14) provides an invaluable, noninvasive imaging technique to map long-range, brain-wide functional connectivity networks based on the temporal coherence of infraslow (0.005-0.1 Hz) blood oxygen level dependent (BOLD) activity. The functional relevance of specific brain-wide networks in co...

Section: Discussionsupporting

confidence: 48%

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Chan

Leong

et al. 2017

“…Furthermore, stronger θ phase-reset with saccades during exploration of a stimulus has been associated with better subsequent recall of that stimulus (36). Thus, the θ phasereset we observe following invalid targets may allow for optimal sensory processing of the unexpected stimulus.…”

Section: Discussionmentioning

confidence: 84%

Frequency-specific mechanism links human brain networks for spatial attention

Daitch¹,

Sharma²,

Roland

et al. 2013

Selective attention allows us to filter out irrelevant information in the environment and focus neural resources on information relevant to our current goals. Functional brain-imaging studies have identified networks of broadly distributed brain regions that are recruited during different attention processes; however, the dynamics by which these networks enable selection are not well understood. Here, we first used functional MRI to localize dorsal and ventral attention networks in human epileptic subjects undergoing seizure monitoring. We subsequently recorded cortical physiology using subdural electrocorticography during a spatialattention task to study network dynamics. Attention networks become selectively phase-modulated at low frequencies (δ, θ) during the same task epochs in which they are recruited in functional MRI. This mechanism may alter the excitability of task-relevant regions or their effective connectivity. Furthermore, different attention processes (holding vs. shifting attention) are associated with synchrony at different frequencies, which may minimize unnecessary cross-talk between separate neuronal processes.O ne of the hallmarks of effective behavior is the ability to flexibly attend to particular stimuli in the environment. Selective attention can be driven endogenously by one's current goals or by salient external stimuli. Human neuroimaging studies have identified two sets of fronto-parietal regions that are recruited during these two types of attention. A set of dorsal fronto-parietal regions (dorsal attention network or DAN) shows sustained activity during endogenous or goal-driven attention (1), and reorienting to unexpected targets transiently activates both the DAN and a second set of regions, the ventral attention network (VAN) (2). Although functional MRI (fMRI) has identified the brain regions that are involved in these attentional operations (3, 4), the slow nature of the hemodynamic response has severely limited the study of network dynamics at behaviorally relevant time scales (5). Here, we report results obtained by cortical surface (electrocorticography or ECoG) recordings in epilepsy patients undergoing clinical monitoring to identify seizure foci. Electrode locations for each subject were colocalized with functional brain networks, including the DAN and VAN identified in the same subjects using fMRI. This experimental paradigm allowed us to objectively link fast electrophysiological dynamics, during performance of an attention task, to well-studied functional brain networks.ECoG measures nonspiking, local field potential oscillations across a range of frequencies, which are thought to reflect fluctuations in local neuronal excitability (6, 7). Phase modulations of activity within a region and between regions may therefore affect, respectively, their ability to respond to inputs and to transfer information between one another (8, 9). In support of this theory, previous studies in both animals and humans have shown that either local or long-distance synchrony change in a tas...

“…The animals performed the VPLT, which was the same as in our previously published work (1,14,42,43). Briefly, a novel set of 200 complex visual images was chosen for each session, and each image was viewed twice while eye position was tracked with an infrared camera (ISCAN).…”

Section: Methodsmentioning

confidence: 99%

Saccade direction encoding in the primate entorhinal cortex during visual exploration

Killian

Potter

Buffalo

2015

Self Cite

We recently demonstrated that position in visual space is represented by grid cells in the primate entorhinal cortex (EC), suggesting that visual exploration of complex scenes in primates may employ signaling mechanisms similar to those used during exploration of physical space via movement in rodents. Here, we describe a group of saccade direction (SD) cells that encode eye movement information in the monkey EC during free-viewing of complex images. Significant saccade direction encoding was found in 20% of the cells recorded in the posterior EC. SD cells were generally broadly tuned and two largely separate populations of SD cells encoded future and previous saccade direction. Some properties of these cells resemble those of head-direction cells in rodent EC, suggesting that the same neural circuitry may be capable of performing homologous spatial computations under different exploratory contexts.