Angular and linear speed cells in the parahippocampal circuits

Spalla, Davide; Treves, Alessandro; Boccara, Charlotte N

doi:10.1038/s41467-022-29583-z

Cited by 22 publications

(16 citation statements)

References 79 publications

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“…Consistent with a recent report (Spalla et al, 2022), we also found that a small proportion of HD cells in each of the parahippocampal areas was modulated by linear velocity (speed), although the proportions were smaller than those reported by Spalla et al In contrast, an even larger proportion of ADN HD cells was modulated by linear velocity (Figure 4). When firing rate versus linear velocity tuning curves were constructed for samples that fell within ±60° of the cell's PFD, the percentage of cells that had linear velocity correlations ≥0.7 (accounting for approximately half of the firing rate variance) and absolute values of slopes ≥0.1 cm/s were PoS: 12.6%, PaS: 4.5%, MEC: 12.1%, POR: 10.0%, and ADN: 33.6%.…”

Section: Resultssupporting

confidence: 92%

Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Clark,

LaChance,

Winter

et al. 2024

Hippocampus

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Head direction (HD) cells, which fire persistently when an animal's head is pointed in a particular direction, are widely thought to underlie an animal's sense of spatial orientation and have been identified in several limbic brain regions. Robust HD cell firing is observed throughout the thalamo‐parahippocampal system, although recent studies report that parahippocampal HD cells exhibit distinct firing properties, including conjunctive aspects with other spatial parameters, which suggest they play a specialized role in spatial processing. Few studies, however, have quantified these apparent differences. Here, we performed a comparative assessment of HD cell firing characteristics across the anterior dorsal thalamus (ADN), postsubiculum (PoS), parasubiculum (PaS), medial entorhinal (MEC), and postrhinal (POR) cortices. We report that HD cells with a high degree of directional specificity were observed in all five brain regions, but ADN HD cells display greater sharpness and stability in their preferred directions, and greater anticipation of future headings compared to parahippocampal regions. Additional analysis indicated that POR HD cells were more coarsely modulated by other spatial parameters compared to PoS, PaS, and MEC. Finally, our analyses indicated that the sharpness of HD tuning decreased as a function of laminar position and conjunctive coding within the PoS, PaS, and MEC, with cells in the superficial layers along with conjunctive firing properties showing less robust directional tuning. The results are discussed in relation to theories of functional organization of HD cell tuning in thalamo‐parahippocampal circuitry.

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Section: Resultssupporting

confidence: 92%

Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Clark,

LaChance,

Winter

et al. 2024

Hippocampus

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“…Although there are differences in the proportion of cells that encode position, head direction and speed between MEC, PrS and PaS (e.g. PrS and PaS have higher proportions of head-direction tuned cells), these regions share a common substrate of spatial/navigational coding (position, head-direction, speed) [6, 15, 16]. We further found a relationship between navigation variables after clustering that revealed an axis of separation along the head-direction and speed coefficients, such that these variables were negatively related.…”

Section: Discussionmentioning

confidence: 99%

“…Both the MEC and PaS contain large populations of neurons that encode navigationally relevant variables for computing an animals spatial position, including: body position, head direction and running speed. Individual MEC neurons often exhibit a mixture in their selectivity for encoding these variables and, while ∼50 % of MEC neurons can be classified based on metrics that quantify the firing rate profile along a behavioral dimension (tuning curves), a larger proportion of neurons can be classified using more unbiased statistical approaches [13][14][15]. In the PaS, ∼50 % of neurons code for heading direction [6,16], with coding for position or running speed present in about ∼40% neurons [15,16].…”

Section: Introductionmentioning

confidence: 99%

“…Individual MEC neurons often exhibit a mixture in their selectivity for encoding these variables and, while ∼50 % of MEC neurons can be classified based on metrics that quantify the firing rate profile along a behavioral dimension (tuning curves), a larger proportion of neurons can be classified using more unbiased statistical approaches [13][14][15]. In the PaS, ∼50 % of neurons code for heading direction [6,16], with coding for position or running speed present in about ∼40% neurons [15,16]. MEC has also been shown to contain neurons that encode variables related to non-spatial features of a task or behavior.…”

Section: Introductionmentioning

confidence: 99%

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Parahippocampal neurons encode task-relevant information for goal-directed navigation

Gonzalez

Giocomo

2022

Preprint

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A behavioral strategy crucial to survival is directed navigation to a goal, such as a food or home location. One potential neural substrate for supporting goal-directed navigation is the parahippocampus, which contains neurons that represent an animals position, orientation, and movement through the world, and that change their firing activity to encode behaviorally relevant variables such as reward. However, little prior work on the parahippocampus has considered how neurons encode variables during goal-directed navigation in environments that dynamically change. Here, we recorded single units from rat parahippocampal cortex while subjects performed a goal-directed task. The maze dynamically changed goal-locations via a visual cue on a trial-to-trial basis, requiring subjects to use cue-location associations to receive reward. We observed a mismatch-like signal, with elevated neural activity on incorrect trials, leading to rate-remapping. The strength of this remapping correlated with task performance. Recordings during open-field foraging allowed us to functionally define navigational coding for a subset of the neurons recorded in the maze. This approach revealed that head-direction coding units remapped more than other functional-defined units. Taken together, this work thus raises the possibility that during goal-directed navigation, parahippocampal neurons encode error information reflective of an animals behavioral performance.

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“…The copyright holder for this preprint this version posted March 31, 2023. ; https://doi.org/10.1101/2023.03.29.534808 doi: bioRxiv preprint 33 Keshavarzi et al, 2022;Spalla et al, 2022). Whether the AHV signal is conveyed to each of these areas via the NPH or SGN, or alternatively via other brainstem areas, awaits further investigation.…”

Section: Comparison To Other Studies In Non-human Primates or Immobil...mentioning

confidence: 99%

Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

Graham

Dumont

Winter

et al. 2023

Preprint

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An animal's perceived sense of orientation depends upon the head direction (HD) system found in several limbic structures and depends upon an intact peripheral vestibular labyrinth. However, how the vestibular system influences the generation, maintenance, and updating of the HD signal remains poorly understood. Anatomical and lesion studies point towards three key brainstem nuclei as being potential critical components in generating the HD signal: nucleus prepositus hypoglossi (NPH), supragenual nucleus (SGN), and dorsal paragigantocellularis reticular nuclei (PGRNd). Collectively, these nuclei are situated between the vestibular nuclei and the dorsal tegmental and lateral mammillary nuclei, which are thought to serve as the origin of the HD signal. To test this hypothesis, extracellular recordings were made in these areas while rats either freely foraged in a cylindrical environment or were restrained and rotated passively. During foraging, a large subset of cells in all three nuclei exhibited activity that correlated with changes in the rat's angular head velocity (AHV). Two fundamental types of AHV cells were observed: 1) symmetrical AHV cells increased or decreased their neural firing with increases in AHV regardless of the direction of rotation; 2) asymmetrical AHV cells responded differentially to clockwise (CW) and counter-clockwise (CCW) head rotations. When rats were passively rotated, some AHV cells remained sensitive to AHV whereas others had attenuated firing. In addition, a large number of AHV cells were modulated by linear head velocity. These results indicate the types of information conveyed in the ascending vestibular pathways that are responsible for generating the HD signal.

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Angular and linear speed cells in the parahippocampal circuits

Cited by 22 publications

References 79 publications

Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Comparison of head direction cell firing characteristics across thalamo‐parahippocampal circuitry

Parahippocampal neurons encode task-relevant information for goal-directed navigation

Angular head velocity cells within brainstem nuclei projecting to the head direction circuit

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