VERVAEKE Koen's profile
avatar

VERVAEKE KoenORCID_LOGO

  • Physiology, University of Oslo, Oslo, Norway
  • Behavioral/Cognitive Neuroscience, Cellular/Molecular Neuroscience, Computational modeling, Electrophysiology, Interneurons, Neuronal oscillations, Plasticity, Rodent model system, Synapse, Synaptic network, Systems/Circuit Neuroscience
  • recommender

Recommendation:  1

Reviews:  0

Areas of expertise
Two photon microscopy.

Recommendation:  1

04 Sep 2024
article picture
POSTPRINT

Multisensory coding of angular head velocity in the retrosplenial cortex

Where was I going? Vestibular-visual integration in the retrosplenial cortex

Recommended by and

We need to keep track of our heading direction, and head direction cells in various brain regions represent exactly that; therefore, they have been identified as key substrates of direction coding. But how is such a variable computed? Head direction representation is thought to arise from the integration of angular velocity, suggesting the existence of angular head velocity (AHV) neurons. Theoretically, vestibular, visual, proprioceptive and motor command signals can all contribute to angular velocity computations, while the actual coding mechanisms have remained unclear.Keshavarzi et al. addressed this by separately controlling vestibular and visual cues in a head-fixed configuration (Keshavarzi et al., 2022b). They targeted the retrosplenial cortex (RSC), a multisensory associational area known to be important for the integration of egocentric and allocentric information during navigation (Solari & Hangya, 2018). The use of high channel-count multielectrode arrays (silicon probes) allowed the authors to track a large number of neurons through different conditions, including free exploration of an open field arena. They identified subsets of neurons representing head direction, AHV, locomotion speed or a combination of these variables.

A large fraction of AHV neurons showed similar tuning properties during free exploration and passive rotation in the dark, demonstrating the importance of vestibular input. In agreement, lesioning the semi-circular canals largely reduced these responses. Next, mice were presented with visual motion stimuli while remaining stationary. This showed that visual signals also contributed to AHV coding and specifically suggested that they increased the gain and improved the signal-to-noise ratio of AHV representations. Mice trained on discriminating rotational stimuli showed improved performance when both visual and vestibular information was available compared to either vestibular-only or visual-only stimuli, further demonstrating the integration of the two types of sensory cues. Finally, the availability of both vestibular and visual information improved decoding accuracy of angular speed from ensembles of retrosplenial cortex neurons compared to single modality stimuli, at least at the beginning of motion.

Keshavarzi et al. provide compelling evidence for the critical role of vestibular input in encoding AHV within the RSC. While the widespread presence of vestibular signals in rodent cortical circuits is well-documented (Rancz et al., 2015), this study significantly advances our understanding by demonstrating that RSC neurons can also encode AHV. These findings align with research that identified AHV representations in the RSC and adjacent cortical regions, including primary visual, secondary visual, posterior parietal, primary motor, secondary motor and primary somatosensory cortices (Hennestad et al., 2021), and with later work that showed AHV in parahippocampal circuits (Spalla et al., 2022).

Notably, the relative contributions of vestibular and visual signals to AHV encoding likely depend on the specific cortical area and the AHV amplitude. Visual flow may be more prominent at lower AHV ranges (0-90 deg/s), while vestibular input likely dominates AHV representation at higher speeds (Stahl, 2004; Hennestad et al., 2021). This suggests a complementary contribution of vestibular and visual information, enabling encoding a broader range of angular velocity and driving a widespread AHV signal across cortical areas.

This is an elegant study in which a creative and clear experimental design helps teasing apart different contributors of a specific computation that normally appear linked during natural behaviors. This way it also demonstrates the power of precise experimental control, while immediately extrapolating to natural behavior by examining the same neurons during free exploration. It additionally demonstrates a non-trivial multisensory integration in the retrosplenial cortex that can directly contribute to egocentric spatial representations during navigation (Alexander & Nitz, 2015, 2017).

 

Editorial note: A preprint version of this article was peer-reviewed by PCI Neuroscience. The refereed preprint can be found through the cited link here (Keshavarzi et al., 2022a), and the peer-review process here.

 

References

Alexander AS, Nitz DA (2015) Retrosplenial cortex maps the conjunction of internal and external spaces. Nature Neuroscience, 18, 1143–1151. https://doi.org/10.1038/nn.4058

Alexander AS, Nitz DA (2017) Spatially Periodic Activation Patterns of Retrosplenial Cortex Encode Route Sub-spaces and Distance Traveled. Current Biology, 27, 1551-1560.e4. https://doi.org/10.1016/j.cub.2017.04.036

Hennestad E, Witoelar A, Chambers AR, Vervaeke K (2021) Mapping vestibular and visual contributions to angular head velocity tuning in the cortex. Cell Reports, 37, 110134. https://doi.org/10.1016/j.celrep.2021.110134

Keshavarzi S, Bracey EF, Faville RA, Campagner D, Tyson AL, Lenzi SC, Branco T, Margrie TW (2022a) The retrosplenial cortex combines internal and external cues to encode head velocity during navigation. https://doi.org/10.5281/zenodo.5834392

Keshavarzi S, Bracey EF, Faville RA, Campagner D, Tyson AL, Lenzi SC, Branco T, Margrie TW (2022b) Multisensory coding of angular head velocity in the retrosplenial cortex. Neuron, 110, 532-543.e9. https://doi.org/10.1016/j.neuron.2021.10.031

Rancz EA, Moya J, Drawitsch F, Brichta AM, Canals S, Margrie TW (2015) Widespread vestibular activation of the rodent cortex. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 35, 5926–5934. https://doi.org/10.1523/JNEUROSCI.1869-14.2015

Solari N, Hangya B (2018) Cholinergic modulation of spatial learning, memory and navigation. European Journal of Neuroscience, 48, 2199–2230. https://doi.org/10.1111/ejn.14089

Spalla D, Treves A, Boccara CN (2022) Angular and linear speed cells in the parahippocampal circuits. Nature Communications, 13, 1907. https://doi.org/10.1038/s41467-022-29583-z

Stahl JS (2004) Using eye movements to assess brain function in mice. Vision Research, 44, 3401–3410. https://doi.org/10.1016/j.visres.2004.09.011

avatar

VERVAEKE KoenORCID_LOGO

  • Physiology, University of Oslo, Oslo, Norway
  • Behavioral/Cognitive Neuroscience, Cellular/Molecular Neuroscience, Computational modeling, Electrophysiology, Interneurons, Neuronal oscillations, Plasticity, Rodent model system, Synapse, Synaptic network, Systems/Circuit Neuroscience
  • recommender

Recommendation:  1

Reviews:  0

Areas of expertise
Two photon microscopy.