Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus

Abstract

Disambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locations in different routes. However, it is unknown how hippocampal neurons disambiguate reward delivery in overlapping path segments in different routes. In the present study, we recorded monkey hippocampal neurons during performance of three virtual navigation (VN) tasks in which a monkey alternately navigated two different routes that included overlapping path segments (common central hallway) and acquired rewards in the same locations in overlapping path segments by manipulating a joystick. The results indicated that out of 106 hippocampal neurons, 57 displayed place-related activity (place-related neurons), and 18 neurons showed route-dependent activity in the overlapping path segments, consistent with a hippocampal role in the disambiguation of overlapping path segments. Moreover, 75 neurons showed neural correlates to reward delivery (reward-related neurons), whereas 56 of these 75 reward-related neurons showed route-dependent reward-related activity in the overlapping path segments. The ensemble activity of reward-related neurons represented reward delivery, locations, and routes in the overlapping path segments. In addition, ensemble activity patterns of hippocampal neurons more distinctly represented overlapping path segments than non-overlapping path segments. The present results provide neurophysiological evidence of disambiguation in the monkey hippocampus, consistent with a hippocampal role in episodic memory, and support a recent computational model of “neural differentiation,” in which overlapping items are better represented by repeated retrieval with competitive learning.

Neural Evidence of Mirror Self-Recognition in the Secondary Somatosensory Cortex of Macaque: Observations from a Single-Cell Recording Experiment and Implications for Consciousness

“…While parietal neurons seem to code a reaching space centered on the head [ 52 , 56 , 57 ], and hippocampal cells code a navigation space based on distal cues and reward locations [ 73 , 74 , 75 ], the SII appears to situate the whole body in the surrounding environment [ 60 ]. As the SII codes not only the separate body parts as a source of somatosensation but also a combination of those body parts into an indivisible concept of an individually and socially aware self-body, both mirror recognition and self/non-self differentiation could be explained along the observed sensory responses.…”

Temporal context and latent state inference in the hippocampal "splitter" signal

“…Although we focus here on spatial trajectories, splitting has also been observed on non-spatial tasks such as those presenting overlapping sequences of discrete odor cues (Ginther et al, 2011;Shahbaba et al, 2022) indicating that the phenomenon is quite general 2 . Similarly, although typical splitter studies use tetrode recordings in rats, trajectory splitting has also been found using calcium imaging in mice (Kinsky et al, 2020;Levy et al, 2021; see also Nieh et al, 2021;Keinath et al, 2020;Sun et al, 2020), using recordings in macaques (Bretas et al, 2019;Gulli et al, 2020) and with intracranial recordings (Ekstrom et al, 2003) and fMRI in humans (Brown et al, 2016(Brown et al, , 2010; see also : Hsieh et al, 2014).…”

Neural basis of topographical disorientation in the primate posterior cingulate gyrus based on a labeled graph

“…The animal sat in a monkey chair with a stereotaxic frame during the recording session. The monkey's head was then painlessly fixed with the stereotaxic frame by fixing a U-shaped frame that was previously implanted into the animal's skull [30] – [33] . During neuronal recording, the left eye positions of the animal were tracked by an eye-tracking system using a CCD camera with a 150 Hz time resolution [34] .…”

“…In the FP-VN task, a 3D open space (diameter, 180 m), which was constructed using 3D software (EON Studio ver. 2.5.2, EON Reality, USA), was used [31] – [33] ( Fig. 1B ).…”

“…1Ca . In this task, to receive liquid rewards, the monkey was required to sequentially visit the reward areas in the fixed sequence; 1) R⇒S⇒C⇒T⇒L (location sequence from 1 to 5; left route), and 2) L⇒S⇒C⇒T⇒R (location sequence from 5 to 9; right route) [33] ( Fig. 1B ).…”