RESUMO
Although much is known about how single neurons in the hippocampus represent an animal's position, how circuit interactions contribute to spatial coding is less well understood. Using a novel statistical estimator and theoretical modeling, both developed in the framework of maximum entropy models, we reveal highly structured CA1 cell-cell interactions in male rats during open field exploration. The statistics of these interactions depend on whether the animal is in a familiar or novel environment. In both conditions the circuit interactions optimize the encoding of spatial information, but for regimes that differ in the informativeness of their spatial inputs. This structure facilitates linear decodability, making the information easy to read out by downstream circuits. Overall, our findings suggest that the efficient coding hypothesis is not only applicable to individual neuron properties in the sensory periphery, but also to neural interactions in the central brain.SIGNIFICANCE STATEMENT Local circuit interactions play a key role in neural computation and are dynamically shaped by experience. However, measuring and assessing their effects during behavior remains a challenge. Here, we combine techniques from statistical physics and machine learning to develop new tools for determining the effects of local network interactions on neural population activity. This approach reveals highly structured local interactions between hippocampal neurons, which make the neural code more precise and easier to read out by downstream circuits, across different levels of experience. More generally, the novel combination of theory and data analysis in the framework of maximum entropy models enables traditional neural coding questions to be asked in naturalistic settings.
Assuntos
Região CA1 Hipocampal , Hipocampo , Ratos , Masculino , Animais , Região CA1 Hipocampal/fisiologia , Neurônios/fisiologia , Rede Nervosa/fisiologiaRESUMO
Aberrant proteostasis of protein aggregation may lead to behavior disorders including chronic mental illnesses (CMI). Furthermore, the neuronal activity alterations that underlie CMI are not well understood. We recorded the local field potential and single-unit activity of the hippocampal CA1 region in vivo in rats transgenically overexpressing the Disrupted-in-Schizophrenia 1 (DISC1) gene (tgDISC1), modeling sporadic CMI. These tgDISC1 rats have previously been shown to exhibit DISC1 protein aggregation, disturbances in the dopaminergic system and attention-related deficits. Recordings were performed during exploration of familiar and novel open field environments and during sleep, allowing investigation of neuronal abnormalities in unconstrained behavior. Compared to controls, tgDISC1 place cells exhibited smaller place fields and decreased speed-modulation of their firing rates, demonstrating altered spatial coding and deficits in encoding location-independent sensory inputs. Oscillation analyses showed that tgDISC1 pyramidal neurons had higher theta phase locking strength during novelty, limiting their phase coding ability. However, their mean theta phases were more variable at the population level, reducing oscillatory network synchronization. Finally, tgDISC1 pyramidal neurons showed a lack of novelty-induced shift in their preferred theta and gamma firing phases, indicating deficits in coding of novel environments with oscillatory firing. By combining single cell and neuronal population analyses, we link DISC1 protein pathology with abnormal hippocampal neural coding and network synchrony, and thereby gain a more comprehensive understanding of CMI mechanisms.
Assuntos
Sincronização Cortical , Hipocampo/fisiologia , Proteínas do Tecido Nervoso/biossíntese , Proteínas do Tecido Nervoso/genética , Animais , Comportamento Animal , Região CA1 Hipocampal/metabolismo , Região CA1 Hipocampal/fisiologia , Eletrodos Implantados , Fenômenos Eletrofisiológicos , Comportamento Exploratório , Ritmo Gama/fisiologia , Hipocampo/metabolismo , Masculino , Células Piramidais/fisiologia , Ratos , Ratos Sprague-Dawley , Descanso/fisiologia , Esquizofrenia/genética , Esquizofrenia/metabolismo , Sono/fisiologiaRESUMO
How the coordination of neuronal spiking and brain rhythms between hippocampal subregions supports memory function remains elusive. We studied the interregional coordination of CA3 neuronal spiking with CA1 theta oscillations by recording electrophysiological signals along the proximodistal axis of the hippocampus in rats that were performing a high-memory-demand recognition memory task adapted from humans. We found that CA3 population spiking occurs preferentially at the peak of distal CA1 theta oscillations when memory was tested but only when previously encountered stimuli were presented. In addition, decoding analyses revealed that only population cell firing of proximal CA3 together with that of distal CA1 can predict performance at test in the present non-spatial task. Overall, our work demonstrates an important role for the synchronization of CA3 neuronal activity with CA1 theta oscillations during memory testing.
Assuntos
Região CA1 Hipocampal , Região CA3 Hipocampal , Memória , Neurônios , Ritmo Teta , Animais , Ritmo Teta/fisiologia , Região CA1 Hipocampal/fisiologia , Masculino , Ratos , Região CA3 Hipocampal/fisiologia , Memória/fisiologia , Neurônios/fisiologia , Potenciais de Ação/fisiologiaRESUMO
Cholecystokinin-expressing interneurons (CCKIs) are hypothesized to shape pyramidal cell-firing patterns and regulate network oscillations and related network state transitions. To directly probe their role in the CA1 region, we silenced their activity using optogenetic and chemogenetic tools in mice. Opto-tagged CCKIs revealed a heterogeneous population, and their optogenetic silencing triggered wide disinhibitory network changes affecting both pyramidal cells and other interneurons. CCKI silencing enhanced pyramidal cell burst firing and altered the temporal coding of place cells: theta phase precession was disrupted, whereas sequence reactivation was enhanced. Chemogenetic CCKI silencing did not alter the acquisition of spatial reference memories on the Morris water maze but enhanced the recall of contextual fear memories and enabled selective recall when similar environments were tested. This work suggests the key involvement of CCKIs in the control of place-cell temporal coding and the formation of contextual memories.
Assuntos
Colecistocinina , Hipocampo , Interneurônios , Optogenética , Células Piramidais , Animais , Masculino , Camundongos , Região CA1 Hipocampal/fisiologia , Região CA1 Hipocampal/citologia , Região CA1 Hipocampal/metabolismo , Colecistocinina/metabolismo , Colecistocinina/genética , Medo/fisiologia , Hipocampo/fisiologia , Interneurônios/fisiologia , Interneurônios/metabolismo , Aprendizagem/fisiologia , Aprendizagem em Labirinto/fisiologia , Memória/fisiologia , Rememoração Mental/fisiologia , Camundongos Endogâmicos C57BL , Camundongos Transgênicos , Células Piramidais/fisiologia , Células Piramidais/metabolismo , Ritmo Teta/fisiologiaRESUMO
The activity of hippocampal pyramidal cells reflects both the current position of the animal and information related to its current behavior. Here we investigated whether single hippocampal neurons can encode several independent features defining trials during a memory task. We also tested whether task-related information is represented by partial remapping of the place cell population or, instead, via firing rate modulation of spatially stable place cells. To address these two questions, the activity of hippocampal neurons was recorded in rats performing a conditional discrimination task on a modified T-maze in which the identity of a food reward guided behavior. When the rat was on the central arm of the maze, the firing rate of pyramidal cells changed depending on two independent factors: (1) the identity of the food reward given to the animal and (2) the previous location of the animal on the maze. Importantly, some pyramidal cells encoded information relative to both factors. This trial-type specific and retrospective coding did not interfere with the spatial representation of the maze: hippocampal cells had stable place fields and their theta-phase precession profiles were unaltered during the task, indicating that trial-related information was encoded via rate remapping. During error trials, encoding of both trial-related information and spatial location was impaired. Finally, we found that pyramidal cells also encode trial-related information via rate remapping during the continuous version of the rewarded alternation task without delays. These results suggest that hippocampal neurons can encode several task-related cognitive aspects via rate remapping.
Assuntos
Potenciais de Ação/fisiologia , Sinais (Psicologia) , Aprendizagem por Discriminação/fisiologia , Hipocampo/citologia , Hipocampo/fisiologia , Aprendizagem em Labirinto/fisiologia , Animais , Masculino , Plasticidade Neuronal/fisiologia , Ratos , Ratos Long-EvansRESUMO
The execution of cognitive functions requires coordinated circuit activity across different brain areas that involves the associated firing of neuronal assemblies. Here, we tested the circuit mechanism behind assembly interactions between the hippocampus and the medial prefrontal cortex (mPFC) of adult rats by recording neuronal populations during a rule-switching task. We identified functionally coupled CA1-mPFC cells that synchronized their activity beyond that expected from common spatial coding or oscillatory firing. When such cell pairs fired together, the mPFC cell strongly phase locked to CA1 theta oscillations and maintained consistent theta firing phases, independent of the theta timing of their CA1 counterpart. These functionally connected CA1-mPFC cells formed interconnected assemblies. While firing together with their CA1 assembly partners, mPFC cells fired along specific theta sequences. Our results suggest that upregulated theta oscillatory firing of mPFC cells can signal transient interactions with specific CA1 assemblies, thus enabling distributed computations.
Assuntos
Hipocampo , Ritmo Teta , Ratos , Animais , Hipocampo/fisiologia , Neurônios/fisiologia , Córtex Pré-Frontal/fisiologiaRESUMO
Hippocampal sharp waves (SPWs) and associated fast ("ripple") oscillations (SPW-Rs) in the CA1 region are among the most synchronous physiological patterns in the mammalian brain. Using two-dimensional arrays of electrodes for recording local field potentials and unit discharges in freely moving rats, we studied the emergence of ripple oscillations (140-220 Hz) and compared their origin and cellular-synaptic mechanisms with fast gamma oscillations (90-140 Hz). We show that (1) hippocampal SPW-Rs and fast gamma oscillations are quantitatively distinct patterns but involve the same networks and share similar mechanisms; (2) both the frequency and magnitude of fast oscillations are positively correlated with the magnitude of SPWs; (3) during both ripples and fast gamma oscillations the frequency of network oscillation is higher in CA1 than in CA3; and (4) the emergence of CA3 population bursts, a prerequisite for SPW-Rs, is biased by activity patterns in the dentate gyrus and entorhinal cortex, with the highest probability of ripples associated with an "optimum" level of dentate gamma power. We hypothesize that each hippocampal subnetwork possesses distinct resonant properties, tuned by the magnitude of the excitatory drive.
Assuntos
Potenciais de Ação/fisiologia , Córtex Entorrinal/fisiologia , Hipocampo/fisiologia , Rede Nervosa/fisiologia , Neurônios/fisiologia , Animais , Eletrofisiologia , Masculino , Ratos , Ratos Long-Evans , Ratos Sprague-DawleyRESUMO
Temporal coding is a means of representing information by the time, as opposed to the rate, at which neurons fire. Evidence of temporal coding in the hippocampus comes from place cells, whose spike times relative to theta oscillations reflect a rat's position while running along stereotyped trajectories. This arises from the backwards shift in cell firing relative to local theta oscillations (phase precession). Here we demonstrate phase precession during place-field crossings in an open-field foraging task. This produced spike sequences in each theta cycle that disambiguate the rat's trajectory through two-dimensional space and can be used to predict movement direction. Furthermore, position and movement direction were maximally predicted from firing in the early and late portions of the theta cycle, respectively. This represents the first direct evidence of a combined representation of position, trajectory and heading in the hippocampus, organized on a fine temporal scale by theta oscillations.
Assuntos
Potenciais de Ação/fisiologia , Relógios Biológicos/fisiologia , Hipocampo/fisiologia , Neurônios/fisiologia , Percepção Espacial/fisiologia , Ritmo Teta , Animais , Comportamento Animal/fisiologia , Comportamento Exploratório/fisiologia , Hipocampo/anatomia & histologia , Masculino , Modelos Estatísticos , Percepção de Movimento/fisiologia , Vias Neurais/fisiologia , Orientação/fisiologia , Ratos , Ratos Long-Evans , Tempo de Reação/fisiologia , Transmissão Sináptica/fisiologia , Fatores de TempoRESUMO
The hippocampus is thought to be involved in episodic memory formation by reactivating traces of waking experience during sleep. Indeed, the joint firing of spatially tuned pyramidal cells encoding nearby places recur during sleep. We found that the sleep cofiring of rat CA1 pyramidal cells encoding similar places increased relative to the sleep session before exploration. This cofiring increase depended on the number of times that cells fired together with short latencies (<50 ms) during exploration, and was strongest between cells representing the most visited places. This is indicative of a Hebbian learning rule in which changes in firing associations between cells are determined by the number of waking coincident firing events. In contrast, cells encoding different locations reduced their cofiring in proportion to the number of times that they fired independently. Together these data indicate that reactivated patterns are shaped by both positive and negative changes in cofiring, which are determined by recent behavior.
Assuntos
Hipocampo/citologia , Hipocampo/fisiologia , Aprendizagem/fisiologia , Células Piramidais/fisiologia , Animais , Comportamento Animal , Eletrodos , Comportamento Exploratório/fisiologia , Ratos , Sono/fisiologia , Fatores de Tempo , Vigília/fisiologiaRESUMO
The mammalian hippocampal formation (HF) plays a key role in several higher brain functions, such as spatial coding, learning and memory. Its simple circuit architecture is often viewed as a trisynaptic loop, processing input originating from the superficial layers of the entorhinal cortex (EC) and sending it back to its deeper layers. Here, we show that excitatory neurons in layer 6b of the mouse EC project to all sub-regions comprising the HF and receive input from the CA1, thalamus and claustrum. Furthermore, their output is characterized by unique slow-decaying excitatory postsynaptic currents capable of driving plateau-like potentials in their postsynaptic targets. Optogenetic inhibition of the EC-6b pathway affects spatial coding in CA1 pyramidal neurons, while cell ablation impairs not only acquisition of new spatial memories, but also degradation of previously acquired ones. Our results provide evidence of a functional role for cortical layer 6b neurons in the adult brain.
Assuntos
Córtex Entorrinal , Potenciais Pós-Sinápticos Excitadores , Hipocampo , Neurônios , Memória Espacial , Animais , Córtex Entorrinal/fisiologia , Potenciais Pós-Sinápticos Excitadores/fisiologia , Hipocampo/fisiologia , Mamíferos , Camundongos , Neurônios/fisiologia , Células Piramidais/fisiologia , Memória Espacial/fisiologiaRESUMO
How seizures start is a major question in epilepsy research. Preictal EEG changes occur in both human patients and animal models, but their underlying mechanisms and relationship with seizure initiation remain unknown. Here we demonstrate the existence, in the hippocampal CA1 region, of a preictal state characterized by the progressive and global increase in neuronal activity associated with a widespread buildup of low-amplitude high-frequency activity (HFA) (>100 Hz) and reduction in system complexity. HFA is generated by the firing of neurons, mainly pyramidal cells, at much lower frequencies. Individual cycles of HFA are generated by the near-synchronous (within approximately 5 ms) firing of small numbers of pyramidal cells. The presence of HFA in the low-calcium model implicates nonsynaptic synchronization; the presence of very similar HFA in the high-potassium model shows that it does not depend on an absence of synaptic transmission. Immediately before seizure onset, CA1 is in a state of high sensitivity in which weak depolarizing or synchronizing perturbations can trigger seizures. Transition to seizure is characterized by a rapid expansion and fusion of the neuronal populations responsible for HFA, associated with a progressive slowing of HFA, leading to a single, massive, hypersynchronous cluster generating the high-amplitude low-frequency activity of the seizure.
Assuntos
Sincronização Cortical , Epilepsia/fisiopatologia , Rede Nervosa/fisiologia , Neurônios/fisiologia , Potenciais de Ação/fisiologia , Animais , Região CA1 Hipocampal/fisiologia , Epilepsia/etiologia , Masculino , Ratos , Ratos Sprague-DawleyRESUMO
We observed sharp wave/ripples (SWR) during exploration within brief (<2.4 s) interruptions of or during theta oscillations. CA1 network responses of SWRs occurring during exploration (eSWR) and SWRs detected in waking immobility or sleep were similar. However, neuronal activity during eSWR was location dependent, and eSWR-related firing was stronger inside the place field than outside. The eSPW-related firing increase was stronger than the baseline increase inside compared to outside, suggesting a "supralinear" summation of eSWR and place-selective inputs. Pairs of cells with similar place fields and/or correlated firing during exploration showed stronger coactivation during eSWRs and subsequent sleep-SWRs. Sequential activation of place cells was not required for the reactivation of waking co-firing patterns; cell pairs with symmetrical cross-correlations still showed reactivated waking co-firing patterns during sleep-SWRs. We suggest that place-selective firing during eSWRs facilitates initial associations between cells with similar place fields that enable place-related ensemble patterns to recur during subsequent sleep-SWRs.
Assuntos
Comportamento Exploratório/fisiologia , Células Piramidais/fisiologia , Percepção Espacial/fisiologia , Potenciais de Ação , Animais , Eletrofisiologia , Masculino , Ratos , Ratos Endogâmicos , Fases do Sono/fisiologia , Ritmo Teta , Vigília/fisiologiaRESUMO
Neurons can produce action potentials with high temporal precision. A fundamental issue is whether, and how, this capability is used in information processing. According to the 'cell assembly' hypothesis, transient synchrony of anatomically distributed groups of neurons underlies processing of both external sensory input and internal cognitive mechanisms. Accordingly, neuron populations should be arranged into groups whose synchrony exceeds that predicted by common modulation by sensory input. Here we find that the spike times of hippocampal pyramidal cells can be predicted more accurately by using the spike times of simultaneously recorded neurons in addition to the animals location in space. This improvement remained when the spatial prediction was refined with a spatially dependent theta phase modulation. The time window in which spike times are best predicted from simultaneous peer activity is 10-30 ms, suggesting that cell assemblies are synchronized at this timescale. Because this temporal window matches the membrane time constant of pyramidal neurons, the period of the hippocampal gamma oscillation and the time window for synaptic plasticity, we propose that cooperative activity at this timescale is optimal for information transmission and storage in cortical circuits.
Assuntos
Potenciais de Ação , Células Piramidais/citologia , Células Piramidais/fisiologia , Animais , Masculino , Ratos , Ratos Sprague-Dawley , Fatores de TempoRESUMO
Temporally organized reactivation of experiences during awake immobility periods is thought to underlie cognitive processes like planning and evaluation. While replay of trajectories is well established for the hippocampus, it is unclear whether the medial prefrontal cortex (mPFC) can reactivate sequential behavioral experiences in the awake state to support task execution. We simultaneously recorded from hippocampal and mPFC principal neurons in rats performing a mPFC-dependent rule-switching task on a plus maze. We found that mPFC neuronal activity encoded relative positions between the start and goal. During awake immobility periods, the mPFC replayed temporally organized sequences of these generalized positions, resembling entire spatial trajectories. The occurrence of mPFC trajectory replay positively correlated with rule-switching performance. However, hippocampal and mPFC trajectory replay occurred independently, indicating different functions. These results demonstrate that the mPFC can replay ordered activity patterns representing generalized locations and suggest that mPFC replay might have a role in flexible behavior. VIDEO ABSTRACT.
Assuntos
Região CA1 Hipocampal/fisiologia , Tomada de Decisões/fisiologia , Neurônios/fisiologia , Córtex Pré-Frontal/fisiologia , Navegação Espacial/fisiologia , Adaptação Psicológica , Animais , Hipocampo/fisiologia , Ratos , VigíliaRESUMO
In vitro work revealed that excitatory synaptic inputs to hippocampal inhibitory interneurons could undergo Hebbian, associative, or non-associative plasticity. Both behavioral and learning-dependent reorganization of these connections has also been demonstrated by measuring spike transmission probabilities in pyramidal cell-interneuron spike cross-correlations that indicate monosynaptic connections. Here we investigated the activity-dependent modification of these connections during exploratory behavior in rats by optogenetically inhibiting pyramidal cell and interneuron subpopulations. Light application and associated firing alteration of pyramidal and interneuron populations led to lasting changes in pyramidal-interneuron connection weights as indicated by spike transmission changes. Spike transmission alterations were predicted by the light-mediated changes in the number of pre- and postsynaptic spike pairing events and by firing rate changes of interneurons but not pyramidal cells. This work demonstrates the presence of activity-dependent associative and non-associative reorganization of pyramidal-interneuron connections triggered by the optogenetic modification of the firing rate and spike synchrony of cells.
Assuntos
Comportamento Exploratório/fisiologia , Hipocampo/fisiologia , Interneurônios/fisiologia , Optogenética , Células Piramidais/fisiologia , Animais , Masculino , Ratos , Ratos Long-EvansRESUMO
Memory consolidation is thought to depend on the reactivation of waking hippocampal firing patterns during sleep. Following goal learning, the reactivation of place cell firing can represent goals and predicts subsequent memory recall. However, it is unclear whether reactivation promotes the recall of the reactivated memories only or triggers wider reorganization. We trained animals to locate goals at fixed locations in two different environments. Following learning, by performing online assembly content decoding, the reactivation of only one environment was disrupted, leading to recall deficit in that environment. The place map of the disrupted environment was destabilized but re-emerged once the goal was relearned. These data demonstrate that sleep reactivation facilitates goal-memory retrieval by strengthening memories that enable the selection of context-specific hippocampal maps. However, sleep reactivation may not be needed for the stabilization of place maps considering that the map of the disrupted environment re-emerged after the retraining of goals.
Assuntos
Hipocampo/fisiopatologia , Transtornos da Memória/fisiopatologia , Animais , Mapeamento Encefálico , Condicionamento Operante , Fenômenos Eletrofisiológicos , Objetivos , Aprendizagem , Consolidação da Memória , Rememoração Mental , Ratos , SonoRESUMO
Hippocampal place cells that fire together within the same cycle of theta oscillations represent the sequence of positions (movement trajectory) that a rat traverses on a linear track. Furthermore, it has been suggested that the encoding of these and other types of temporal memory sequences is organized by gamma oscillations nested within theta oscillations. Here, we examined whether gamma-related firing of place cells permits such discrete temporal coding. We found that gamma-modulated CA1 pyramidal cells separated into two classes on the basis of gamma firing phases during waking theta periods. These groups also differed in terms of their spike waveforms, firing rates, and burst firing tendency. During gamma oscillations one group's firing became restricted to theta phases associated with the highest gamma power. Consequently, on the linear track, cells in this group often failed to fire early in theta-phase precession (as the rat entered the place field) if gamma oscillations were present. The second group fired throughout the theta cycle during gamma oscillations, and maintained gamma-modulated firing at different stages of theta-phase precession. Our results suggest that the two different pyramidal cell classes may support different types of population codes within a theta cycle: one in which spike sequences representing movement trajectories occur across subsequent gamma cycles nested within each theta cycle, and another in which firing in synchronized gamma discharges without temporal sequences encode a representation of location. We propose that gamma oscillations during theta-phase precession organize the mnemonic recall of population patterns representing places and movement paths.
Assuntos
Potenciais de Ação/fisiologia , Relógios Biológicos/fisiologia , Hipocampo/citologia , Células Piramidais/fisiologia , Animais , Comportamento Animal , Interneurônios/fisiologia , Masculino , Ratos , Sono/fisiologia , Análise Espectral , Vigília/fisiologiaRESUMO
In the subthalamic nucleus (STN) of Parkinson's disease (PD) patients, a pronounced synchronization of oscillatory activity at beta frequencies (15-30 Hz) accompanies movement difficulties. Abnormal beta oscillations and motor symptoms are concomitantly and acutely suppressed by dopaminergic therapies, suggesting that these inappropriate rhythms might also emerge acutely from disrupted dopamine transmission. The neural basis of these abnormal beta oscillations is unclear, and how they might compromise information processing, or how they arise, is unknown. Using a 6-hydroxydopamine-lesioned rodent model of PD, we demonstrate that beta oscillations are inappropriately exaggerated, compared with controls, in a brain-state-dependent manner after chronic dopamine loss. Exaggerated beta oscillations are expressed at the levels of single neurons and small neuronal ensembles, and are focally present and spatially distributed within STN. They are also expressed in synchronous population activities, as evinced by oscillatory local field potentials, in STN and cortex. Excessively synchronized beta oscillations reduce the information coding capacity of STN neuronal ensembles, which may contribute to parkinsonian motor impairment. Acute disruption of dopamine transmission in control animals with antagonists of D(1)/D(2) receptors did not exaggerate STN or cortical beta oscillations. Moreover, beta oscillations were not exaggerated until several days after 6-hydroxydopamine injections. Thus, contrary to predictions, abnormally amplified beta oscillations in cortico-STN circuits do not result simply from an acute absence of dopamine receptor stimulation, but are instead delayed sequelae of chronic dopamine depletion. Targeting the plastic processes underlying the delayed emergence of pathological beta oscillations after continuing dopaminergic dysfunction may offer considerable therapeutic promise.
Assuntos
Ritmo beta , Córtex Cerebral/fisiologia , Dopamina/metabolismo , Núcleo Subtalâmico/fisiologia , Análise de Variância , Animais , Benzazepinas/farmacologia , Ritmo beta/efeitos dos fármacos , Córtex Cerebral/efeitos dos fármacos , Córtex Cerebral/lesões , Antagonistas de Dopamina/farmacologia , Masculino , Oxidopamina/toxicidade , Racloprida/farmacologia , Ratos , Ratos Sprague-Dawley , Análise Espectral , Estatísticas não Paramétricas , Núcleo Subtalâmico/efeitos dos fármacos , Núcleo Subtalâmico/lesões , Simpatolíticos/toxicidade , Fatores de Tempo , VigíliaRESUMO
Hippocampal activity patterns representing movement trajectories are reactivated in immobility and sleep periods, a process associated with memory recall, consolidation, and decision making. It is thought that only fixed, behaviorally relevant patterns can be reactivated, which are stored across hippocampal synaptic connections. To test whether some generalized rules govern reactivation, we examined trajectory reactivation following non-stereotypical exploration of familiar open-field environments. We found that random trajectories of varying lengths and timescales were reactivated, resembling that of Brownian motion of particles. The animals' behavioral trajectory did not follow Brownian diffusion demonstrating that the exact behavioral experience is not reactivated. Therefore, hippocampal circuits are able to generate random trajectories of any recently active map by following diffusion dynamics. This ability of hippocampal circuits to generate representations of all behavioral outcome combinations, experienced or not, may underlie a wide variety of hippocampal-dependent cognitive functions such as learning, generalization, and planning.
Assuntos
Cognição/fisiologia , Comportamento Exploratório/fisiologia , Hipocampo/fisiologia , Animais , Comportamento Apetitivo , Comportamento Animal , Região CA1 Hipocampal/fisiologia , Generalização Psicológica , Aprendizagem , Memória , Vias Neurais/fisiologia , Ratos , Ratos Long-Evans , Reconhecimento PsicológicoRESUMO
Hippocampus is needed for both spatial working and reference memories. Here, using a radial eight-arm maze, we examined how the combined demand on these memories influenced CA1 place cell assemblies while reference memories were partially updated. This was contrasted with control tasks requiring only working memory or the update of reference memory. Reference memory update led to the reward-directed place field shifts at newly rewarded arms and to the gradual strengthening of firing in passes between newly rewarded arms but not between those passes that included a familiar-rewarded arm. At the maze center, transient network synchronization periods preferentially replayed trajectories of the next chosen arm in reference memory tasks but the previously visited arm in the working memory task. Hence, reference memory demand was uniquely associated with a gradual, goal novelty-related reorganization of place cell assemblies and with trajectory replay that reflected the animal's decision of which arm to visit next.