Steven Poulter

Durham University

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The Neurobiology of Mammalian Navigation

Current Biology (2018)

Steven Poulter Tom T. Hartley Colin Lever

Mammals have evolved specialized brain systems to support efficient navigation within diverse habitats and over varied distances, but while navigational strategies and sensory mechanisms vary across species, core spatial components appear to be widely shared. This review presents common elements found in mammalian spatial mapping systems, focusing on the cells in the hippocampal formation representing orientational and locational spatial information, and 'core' mammalian hippocampal circuitry. Mammalian spatial mapping systems make use of both allothetic cues (space-defining cues in the external environment) and idiothetic cues (cues derived from self-motion). As examples of each cue type, we discuss: environmental boundaries, which control both orientational and locational neuronal activity and behaviour; and 'path integration', a process that allows the estimation of linear translation from velocity signals, thought to depend upon grid cells in the entorhinal cortex. Building cognitive maps entails sampling environments: we consider how the mapping system controls exploration to acquire spatial information, and how exploratory strategies may integrate idiothetic with allothetic information. We discuss how 'replay' may act to consolidate spatial maps, and simulate trajectories to aid navigational planning. Finally, we discuss grid cell models of vector navigation.

10.1016/j.cub.2018.05.050

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Citations (155)

Dorsolateral striatal lesions impair navigation based on landmark-goal vectors but facilitate spatial learning based on a “cognitive map”

Learning & Memory (2015)

Yutaka Kosaki Steven Poulter Joseph M. Austen Anthony McGregor

In three experiments, the nature of the interaction between multiple memory systems in rats solving a variation of a spatial task in the water maze was investigated. Throughout training rats were able to find a submerged platform at a fixed distance and direction from an intramaze landmark by learning a landmark-goal vector. Extramaze cues were also available for standard place learning, or “cognitive mapping,” but these cues were valid only within each session, as the position of the platform moved around the pool between sessions together with the intramaze landmark. Animals could therefore learn the position of the platform by taking the consistent vector from the landmark across sessions or by rapidly encoding the new platform position on each session with reference to the extramaze cues. Excitotoxic lesions of the dorsolateral striatum impaired vector-based learning but facilitated cognitive map-based rapid place learning when the extramaze cues were relatively poor (Experiment 1) but not when they were more salient (Experiments 2 and 3). The way the lesion effects interacted with cue availability is consistent with the idea that the memory systems involved in the current navigation task are functionally cooperative yet associatively competitive in nature.

Landmark

Cognitive map

Sensory cue

Water maze

10.1101/lm.037077.114

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Citations (43)

Faculty Opinions recommendation of Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2020)

Colin Lever Steven Poulter

BACKGROUND: There is no consensus about which hippocampal subfields become atrophic earliest in the course of Alzheimer's disease (AD).METHODS: Thirty AD patients, 41 mild cognitive impairment (MCI) patients, and 38 healthy controls (HCs) underwent cerebral magnetic resonance imaging (with an automated segmentation protocol for the volumetric analysis of hippocampal subfields) and a test of immediate and delayed recall of a 15-word list.RESULTS: The volumes of the presubiculum and subiculum presented the most remarkable reduction in the patient's groups. In the MCI group, only the volumes of presubiculum and subiculum predicted performance on the memory tests. In AD patients, the volumes of all hippocampal subfields (with the notable exception of the CA1) predicted memory scores.CONCLUSIONS: Our data point to a prevalent atrophy of the presubicular-subicular complex from the early phases of AD. This finding is consistent with neuropathological observations in AD patients and probably reflects the severe degeneration of the perforant pathway while penetrating the hippocampus through the subicular field in its course from the entorhinal cortex to the dentate gyrus. PMID: 27239489

Subiculum

Entorhinal cortex

Perforant Pathway

10.3410/f.733246270.793571962

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Author response for "Neural correlates of distinct levels of predatory threat in dorsal periaqueductal gray neurons"

Ricardo P. Bindi Ricardo G. O. Maia Francesca Pibiri Marcus Vinícius C. Baldo Steven Poulter

Gray (unit)

Periaqueductal gray

Neural Activity

10.1111/ejn.15633/v3/response1

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Faculty Opinions recommendation of Absence of visual input results in the disruption of grid cell firing in the mouse.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2016)

Colin Lever Steven Poulter

Grid cell

10.3410/f.726619954.793524806

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Frequency matters: how changes in hippocampal theta frequency can influence temporal coding, anxiety-reduction, and memory

Frontiers in Systems Neuroscience (2023)

Miranda Hines Steven Poulter Vincent Douchamps Francesca Pibiri Anthony McGregor

Hippocampal theta frequency is a somewhat neglected topic relative to theta power, phase, coherence, and cross-frequency coupling. Accordingly, here we review and present new data on variation in hippocampal theta frequency, focusing on functional associations (temporal coding, anxiety reduction, learning, and memory). Taking the rodent hippocampal theta frequency to running-speed relationship as a model, we identify two doubly-dissociable frequency components: (a) the slope component of the theta frequency-to-stimulus-rate relationship ("theta slope"); and (b) its y-intercept frequency ("theta intercept"). We identify three tonic determinants of hippocampal theta frequency. (1) Hotter temperatures increase theta frequency, potentially consistent with time intervals being judged as shorter when hot. Initial evidence suggests this occurs via the "theta slope" component. (2) Anxiolytic drugs with widely-different post-synaptic and pre-synaptic primary targets share the effect of reducing the "theta intercept" component, supporting notions of a final common pathway in anxiety reduction involving the hippocampus. (3) Novelty reliably decreases, and familiarity increases, theta frequency, acting upon the "theta slope" component. The reliability of this latter finding, and the special status of novelty for learning, prompts us to propose a Novelty Elicits Slowing of Theta frequency (NEST) hypothesis, involving the following elements: (1) Theta frequency slowing in the hippocampal formation is a generalised response to novelty of different types and modalities; (2) Novelty-elicited theta slowing is a hippocampal-formation-wide adaptive response functioning to accommodate the additional need for learning entailed by novelty; (3) Lengthening the theta cycle enhances associativity; (4) Even part-cycle lengthening may boost associativity; and (5) Artificial theta stimulation aimed at enhancing learning should employ low-end theta frequencies.

10.3389/fnsys.2022.998116

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Citations (6)

Faculty Opinions recommendation of Dynamics of place, boundary and object encoding in rat anterior claustrum.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2015)

Colin Lever Steven Poulter

Claustrum

Dynamics

10.3410/f.725895126.793510841

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The within-subject application of diffusion tensor MRI and CLARITY reveals brain structural changes inNrxn2deletion mice

bioRxiv (Cold Spring Harbor Laboratory) (2018)

Eleftheria Pervolaraki Adam L. Tyson Francesca Pibiri Steven Poulter Amy C. Reichelt

Abstract Background Of the many genetic mutations known to increase the risk of autism spectrum disorder, a large proportion cluster upon synaptic proteins. One such family of presynaptic proteins are the neurexins (NRXN), and recent genetic and mouse evidence has suggested a causative role for NRXN2 in generating altered social behaviours. Autism has been conceptualised as a disorder of atypical connectivity, yet how single-gene mutations affect such connectivity remains under-explored. To attempt to address this, we have developed a quantitative analysis of microstructure and structural connectivity leveraging diffusion tensor MRI (DTI) with high-resolution 3D imaging in optically cleared (CLARITY) brain tissue in the same mouse, applied here to the Nrxn2α knockout (KO) model. Methods Fixed brains of Nrxn2α KO mice underwent DTI using 9.4T MRI, and diffusion properties of socially-relevant brain regions were quantified. The same tissue was then subjected to CLARITY to immunolabel axons and cell bodies, which were also quantified. Results DTI revealed decreases in fractional anisotropy and increases in apparent diffusion coefficient in the amygdala (including the basolateral nuclei), the anterior cingulate cortex, the orbitofrontal cortex and the hippocampus. Radial diffusivity of the anterior cingulate cortex and orbitofrontal cortex was significantly increased in Nrxn2α KO mice, as were tracts between the amygdala and the orbitofrontal cortex. Using CLARITY, we find significantly altered axonal orientation in the amygdala, orbitofrontal cortex and the anterior cingulate cortex, which was unrelated to cell density. Conclusions Our findings demonstrate that deleting a single neurexin gene ( Nrxn2α ) induces atypical structural connectivity within socially-relevant brain regions. More generally, our combined within-subject DTI and CLARITY approach presents a new, more sensitive method of revealing hitherto undetectable differences in the autistic brain.

Orbitofrontal cortex

Posterior cingulate

10.1101/300806

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Citations (2)

Neural correlates of distinct levels of predatory threat in dorsal periaqueductal grey neurons

European Journal of Neuroscience (2022)

Ricardo P. Bindi Ricardo G. O. Maia Francesca Pibiri Marcus Vinícius C. Baldo Steven Poulter

Abstract The dorsal periaqueductal grey (PAG) is an important site for integrating predatory threats. However, it remains unclear whether predator‐related activation in PAG primarily reflects threat itself and thus can distinguish between various degrees of threat, or rather reflects threat‐oriented behaviours, with the PAG potentially orchestrating different types of defensive repertoire. To address this issue, we performed extracellular recording of dorsal PAG neurons in freely behaving rats and examined neuronal and behavioural responses to stimulus conditions with distinct levels of predatory threat. Animals were sequentially exposed to a nonthreatening stimulus familiar environment (exposure to habituated environment) and to a novel nonthreatening stimulus (i.e., a toy animal—plush) and to conditions with high (exposure to a live cat), intermediate (exposure to the environment just visited by the cat, with remnant predator scent), and low (exposure on the following day to the predatory context) levels of predatory threat. To test for contributions of both threat stimuli and behaviour to changes in firing rate, we applied a Poisson generalized linear model regression, using the different predator stimulus conditions and defensive repertoires as predictor variables. Analysis revealed that the different predator stimulus conditions were more predictive of changes in firing rate (primarily threat‐induced increases) than the different defensive repertoires. Thus, the dorsal PAG may code for different levels of predatory threat, more than it directly orchestrates distinct threat‐oriented behaviours. The present results open interesting perspectives to investigate the role of the dorsal PAG in mediating primal emotional and cognitive responses to fear‐inducing stimuli.

Stimulus (psychology)

Escape response

Periaqueductal gray

10.1111/ejn.15633

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Citations (8)

Faculty Opinions recommendation of Distinct Transcriptomic Cell Types and Neural Circuits of the Subiculum and Prosubiculum along the Dorsal-Ventral Axis.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2020)

Colin Lever Steven Poulter

Subiculum

Biological neural network

10.3410/f.737989388.793575654

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