RESUMEN
The spatial mapping function of the hippocampal formation is likely derived from two sets of information: one based on the external environment and the other based on self-motion. Here, we further characterize 'boundary vector cells' (BVCs) in the rat subiculum, which code space relative to one type of cue in the external environment: boundaries. We find that the majority of cells with fields near the perimeter of a walled environment exhibit an additional firing field when an upright barrier is inserted into the walled environment in a manner predicted by the BVC model. We use this property of field repetition as a heuristic measure to define BVCs, and characterize their spatial and temporal properties. In further tests, we find that subicular BVCs typically treat drop edges similarly to walls, including exhibiting field repetition when additional drop-type boundaries are added to the testing environment. In other words, BVCs treat both kinds of edge as environmental boundaries, despite their dissimilar sensory properties. Finally, we also report the existence of 'boundary-off cells', a new class of boundary-coding cells. These cells fire everywhere except where a given BVC might fire.
Asunto(s)
Señales (Psicología) , Potenciales Evocados/fisiología , Hipocampo/fisiología , Modelos Neurológicos , Neuronas/fisiología , Percepción Espacial/fisiología , Animales , Simulación por Computador , Electrofisiología/métodos , Hipocampo/citología , Masculino , Método de Montecarlo , RatasRESUMEN
Hippocampal processing is strongly implicated in both spatial cognition and anxiety and is temporally organized by the theta rhythm. However, there has been little attempt to understand how each type of processing relates to the other in behaving animals, despite their common substrate. In freely moving rats, there is a broadly linear relationship between hippocampal theta frequency and running speed over the normal range of speeds used during foraging. A recent model predicts that spatial-translation-related and arousal/anxiety-related mechanisms of hippocampal theta generation underlie dissociable aspects of the theta frequency-running speed relationship (the slope and intercept, respectively). Here we provide the first confirmatory evidence: environmental novelty decreases slope, whereas anxiolytic drugs reduce intercept. Variation in slope predicted changes in spatial representation by CA1 place cells and novelty-responsive behavior. Variation in intercept predicted anxiety-like behavior. Our findings isolate and doubly dissociate two components of theta generation that operate in parallel in behaving animals and link them to anxiolytic drug action, novelty, and the metric for self-motion.
Asunto(s)
Ansiolíticos/farmacología , Conducta Exploratoria/fisiología , Hipocampo/efectos de los fármacos , Ritmo Teta/fisiología , Vigilia/fisiología , Análisis de Varianza , Animales , Ansiedad/tratamiento farmacológico , Ansiedad/etiología , Temperatura Corporal/efectos de los fármacos , Modelos Animales de Enfermedad , Relación Dosis-Respuesta a Droga , Electroencefalografía , Potenciales Evocados/efectos de los fármacos , Conducta Exploratoria/efectos de los fármacos , Hipocampo/fisiología , Masculino , Ratas , Percepción Espacial/efectos de los fármacos , Percepción Espacial/fisiología , Ritmo Teta/efectos de los fármacos , Factores de Tiempo , Vigilia/efectos de los fármacosRESUMEN
The formation of new memories requires new information to be encoded in the face of proactive interference from the past. Two solutions have been proposed for hippocampal region CA1: (1) acetylcholine, released in novelty, selectively suppresses excitatory projections to CA1 from CA3 (mediating the products of retrieval), while sparing entorhinal inputs (mediating novel sensory information) and (2) encoding preferentially occurs at the pyramidal-layer theta peak, coincident with input from entorhinal cortex, and retrieval occurs at the trough, coincident with input from CA3, consistent with theta phase-dependent synaptic plasticity. We examined three predictions of these models: (1) in novel environments, the preferred theta phase of CA1 place cell firing should shift closer to the CA1 pyramidal-layer theta peak, shifting the encoding-retrieval balance toward encoding; (2) the encoding-related shift in novel environments should be disrupted by cholinergic antagonism; and (3) in familiar environments, cholinergic antagonism should shift the preferred theta firing phase closer to the theta trough, shifting the encoding-retrieval balance even further toward retrieval. We tested these predictions by recording from CA1 pyramidal cells in freely moving rats as they foraged in open field environments under the influence of scopolamine (an amnestic cholinergic antagonist) or vehicle (saline). Results confirmed all three predictions, supporting both the theta phase and cholinergic models of encoding versus retrieval dynamics. Also consistent with cholinergic enhancement of encoding, scopolamine attenuated the formation of distinct spatial representations in a new environment, reducing the extent of place cell "remapping."
Asunto(s)
Acetilcolina/metabolismo , Hipocampo/fisiología , Recuerdo Mental/fisiología , Modelos Neurológicos , Reconocimiento en Psicología/fisiología , Ritmo Teta/fisiología , Potenciales de Acción/efectos de los fármacos , Potenciales de Acción/fisiología , Análisis de Varianza , Animales , Antagonistas Colinérgicos/farmacología , Electroencefalografía , Hipocampo/anatomía & histología , Hipocampo/citología , Hipocampo/efectos de los fármacos , Masculino , Recuerdo Mental/efectos de los fármacos , Neuronas/efectos de los fármacos , Neuronas/fisiología , Ratas , Reconocimiento en Psicología/efectos de los fármacos , Escopolamina/farmacología , Ritmo Teta/efectos de los fármacosRESUMEN
The mechanism supporting the role of the hippocampal formation in novelty detection remains controversial. A comparator function has been variously ascribed to CA1 or subiculum, whereas the theta rhythm has been suggested to separate neural firing into encoding and retrieval phases. We investigated theta phase of firing in principal cells in subiculum and CA1 as rats foraged in familiar and novel environments. We found that the preferred theta phase of firing in CA1, but not subiculum, was shifted to a later phase of the theta cycle during environmental novelty. Furthermore, the amount of phase shift elicited by environmental change correlated with the extent of place cell remapping in CA1. Our results support a relationship between theta phase and novelty-induced plasticity in CA1.
Asunto(s)
Potenciales de Acción , Región CA1 Hipocampal/fisiología , Ambiente , Hipocampo/fisiología , Percepción Espacial/fisiología , Ritmo Teta , Análisis de Varianza , Animales , Electroencefalografía , Neuronas/fisiología , RatasRESUMEN
"Boundary vector cells" were predicted to exist by computational models of the environmental inputs underlying the spatial firing patterns of hippocampal place cells (O'Keefe and Burgess, 1996; Burgess et al., 2000; Hartley et al., 2000). Here, we report the existence of cells fulfilling this description in recordings from the subiculum of freely moving rats. These cells may contribute environmental information to place cell firing, complementing path integrative information. Their relationship to other cell types, including medial entorhinal "border cells," is discussed.