Hippocampal global remapping for different sensory modalities in flying bats

Abstract

Hippocampal place cells encode the animal's spatial position. However, it is unknown how different long-range sensory systems affect spatial representations. Here we alternated usage of vision and echolocation in Egyptian fruit bats while recording from single neurons in hippocampal areas CA1 and subiculum. Bats flew back and forth along a linear flight track, employing echolocation in darkness or vision in light. Hippocampal representations remapped between vision and echolocation via two kinds of remapping: subiculum neurons turned on or off, while CA1 neurons shifted their place fields. Interneurons also exhibited strong remapping. Finally, hippocampal place fields were sharper under vision than echolocation, matching the superior sensory resolution of vision over echolocation. Simulating several theoretical models of place-cells suggested that combining sensory information and path integration best explains the experimental sharpening data. In summary, here we show sensory-based global remapping in a mammal, suggesting that the hippocampus does not contain an abstract spatial map but rather a 'cognitive atlas', with multiple maps for different sensory modalities.

Context-dependent spatially periodic activity in the human entorhinal cortex

“…The observed proportion of neurons with spatial tuning is consistent with data from the rat EC (11), but larger than observed in the primate EC during visual tasks (35) and in the human EC during other virtual navigation tasks (31). Because our electrodes were nonmoveable, selective sampling could not bias this ratio.…”

“…Neurons in CA1 and CA3 remap their place fields upon changes made in the environment, as demonstrated in rodents (13)(14)(15)(16)(17), Chiroptera (35), and primates (36). Because the adaptive remapping of hippocampal place fields is a relatively fast and EC-dependent process (13,37), it is plausible to assume that neurons in the EC are endowed with some degree of flexibility.…”

“…Third, considering the complexity and scalability of human environments, humans might rely on extracting information from optic flow more efficiently than rats do, given that there is theoretically sufficient information available from optic flow for grid formation (45). The predominance of visual input in the human brain allows detection and mapping of spatial cues more quickly and may influence grid parameters to a greater degree than is possible in the rat brain (35)(36)(37). It might also allow the human hippocampus and EC to perform more naturally in virtual navigation tasks, where proprioceptive and kinesthetic cues are absent (30,31,46,47).…”

The influence of low-level stimulus features on the representation of contexts, items, and their mnemonic associations

“…Geva-Sagiv et al (2016) recorded from the bat hippocampus (CA1 and subiculum) and provided evidence that place cell maps between vision- and echolocation-based navigation of the same environment are unrelated, raising questions about whether place cells represent the neural instantiation of an invariant spatial map or whether they contain sensory-specific signals. Additionally, studies in the rodent that have recorded simultaneously from V1 and the hippocampus have shown “place cell” activity in V1 (Ji and Wilson, 2007), which was also shown to precede place cell activity in the hippocampus (Haggerty and Ji, 2015).…”

Three brain states in the hippocampus and cortex

“…This was initially indicated in environments with linear paths, where it was found that place cells often fire only in one direction of travel (McNaughton et al, ), thus ruling out purely spatial representation. Subsequent work has found that a variety of additional variables have roles in determining the place representation (in short, variables based on task, memory, behavior, motivational state, sensory modality, and nonspatial cues; reviewed in Eichenbaum et al (); Shapiro et al (); O'Keefe (); Eichenbaum and Cohen (); Eichenbaum ()); also see recent relevant work [Geva‐Sagiv, Romani, Las, & Ulanovsky, ; Sarel, Finkelstein, Las, & Ulanovsky, ; Danjo, Toyoizumi, & Fujisawa, ; Omer, Maimon, Las, & Ulanovsky, ]).…”