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Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus.

ABSTRACT: Throughout life animals inevitably encounter unforeseen threatening events. Activity of principal cells in the hippocampus is tuned for locations and for salient stimuli in the animals' environment thus forming a map known to be pivotal for guiding behavior. Here, we explored if a code of threatening stimuli exists in the CA1 region of the dorsal hippocampus of mice by recording neuronal response to aversive stimuli delivered at changing locations. We have discovered a rapidly emerging, location independent response to innoxious aversive stimuli composed of the coordinated activation of subgroups of pyramidal cells and connected interneurons. Activated pyramidal cells had higher basal firing rate, more probably participated in ripples, targeted more interneurons than place cells and many of them lacked place fields. We also detected aversive stimulus-coupled assemblies dominated by the activated neurons. Notably, these assemblies could be observed even before the delivery of the first aversive event. Finally, we uncovered the systematic shift of the spatial code from the aversive to, surprisingly, the reward location during the fearful stimulus. Our results uncovered components of the dorsal CA1 circuit possibly key for re-sculpting the spatial map in response to abrupt aversive events.

SUBMITTER: Barth AM

PROVIDER: S-EPMC10611787 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus.

Barth Albert M AM Jelitai Marta M Vasarhelyi-Nagy Maria Flora MF Varga Viktor V

Nature communications 20231027 1

Throughout life animals inevitably encounter unforeseen threatening events. Activity of principal cells in the hippocampus is tuned for locations and for salient stimuli in the animals' environment thus forming a map known to be pivotal for guiding behavior. Here, we explored if a code of threatening stimuli exists in the CA1 region of the dorsal hippocampus of mice by recording neuronal response to aversive stimuli delivered at changing locations. We have discovered a rapidly emerging, location ...[more]

PMID: 37891171

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Project description:Specific memory processes and neurological disorders can be ascribed to different dorsoventral regions of the hippocampus. Recently, differences in the anatomical and physiological properties between dorsal and ventral hippocampal CA1 neurons were described for both the rat and mouse hippocampus and have greatly contributed to our understanding of these processes. While differences in the subthreshold properties were similar between rat and mouse neurons, differences in action potential output between dorsal and ventral neurons were strikingly less divergent in mouse compared with rat CA1 neurons. Here, we investigate the mechanism underlying the lack of difference in action potential firing between dorsal and ventral CA1 pyramidal neurons in mouse hippocampus. Consistent with rat, we found that ventral CA1 neurons had a more depolarized resting membrane potential and higher input resistance than dorsal CA1 neurons in the mouse hippocampus. Despite these differences, action potential output in response to current injection was not significantly different. We found that ventral neurons have a more depolarized action potential threshold compared with dorsal neurons and that threshold in ventral neurons was more sensitive to block of KV1 channels compared with dorsal neurons. Outside-out voltage-clamp recordings found that slowly inactivating K+ currents were larger in ventral CA1 neurons. These results suggest that, despite differences in subthreshold properties between dorsal and ventral CA1 neurons, action potential output is normalized by the differential functional expression of D-type K+ channels. NEW & NOTEWORTHY Understanding differences in neurons within a brain region is integral in the reliable interpretation of comparative studies. Our findings identify a novel mechanism by which D-type potassium channels normalize action potential firing between dorsal and ventral CA1 neurons of mouse hippocampus despite differences in subthreshold intrinsic properties. Action potential threshold in ventral neurons is influenced by a greater functional expression of D-type potassium channels resulting in a depolarized action potential threshold compared with dorsal hippocampus.

Project description:BackgroundThe functional heterogeneity of the hippocampus along its longitudinal axis at the level of behavior is an established concept; however, the neurobiological mechanisms are still unknown. Diversifications in the functioning of intrinsic hippocampal circuitry including short-term dynamics of synaptic inputs and neuronal output, that are important determinants of information processing in the brain, may profoundly contribute to functional specializations along the hippocampus. The objectives of the present study were the examination of the role of the GABAA receptor-mediated inhibition, the μ-opioid receptors and the effect of stimulation intensity on the dynamics of both synaptic input and neuronal output of CA1 region in the dorsal and ventral hippocampus. We used recordings of field potentials from adult rat hippocampal slices evoked by brief repetitive activation of Schaffer collaterals.ResultsWe find that the local CA1 circuit of the dorsal hippocampus presents a remarkably increased dynamic range of frequency-dependent short-term changes in both input and output, ranging from strong facilitation to intense depression at low and high stimulation frequencies respectively. Furthermore, the input-output relationship in the dorsal CA1 circuit is profoundly influenced by frequency and time of presynaptic activation. Strikingly, the ventral hippocampus responds mostly with depression, displaying a rather monotonous input-output relationship over frequency and time. Partial blockade of GABAA receptor-mediated transmission (by 5 μM picrotoxin) profoundly influences input and output dynamics in the dorsal hippocampus but affected only the neuronal output in the ventral hippocampus. M-opioid receptors control short-term dynamics of input and output in the dorsal hippocampus but they play no role in the ventral hippocampus.ConclusionThe results demonstrate that information processing by CA1 local network is highly diversified between the dorsal and ventral hippocampus. Transient detection of incoming patterns of activity and frequency-dependent sustained signaling of amplified neuronal information may be assigned to the ventral and dorsal hippocampal circuitry respectively. This disparity should have profound implications for the functional roles ascribed to distinct segments along the long axis of the hippocampus.

Dataset Information

Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus.

Publications

Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus.

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