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Matthew L Shapiro

Publications and source records attributed to Matthew L Shapiro.

6 recordsLinked to original sources

Representing episodes in the mammalian brain.

Memory lets the past inform the present so that we can attain future goals. In many species, these abilities require the hippocampus. Recent experiments, in which memory demand was varied while overt behavior and the environment were kept constant, have revealed firing patterns of hippocampal neurons that corresponded with memory demands and predicted performance. Although the active population appeared to be 'place cells' that signalled location, it actually included cells the activity patterns of which distinguished the recent or pending history of behavior during identical actions that occurred in the same place. Different populations of hippocampal cells fired as a rat walked along the same spatial path on the way to different goals, and coded past, present and pending events. Other experiments provide converging data that neuronal activity is modulated by goal-directed behavioral episodes. Together, these firing patterns suggest a testable mechanism of episodic memory coding: that hippocampal dynamics encode a temporally extended, hierarchically organized representation of goal-directed behavior.

Action Potentials↗

Relative spike timing in pairs of hippocampal neurons distinguishes the beginning and end of journeys.

Episodic memory organizes experience in time, so that we can review past events and anticipate the future. In a hippocampus-dependent memory task, spike timing in pairs of simultaneously active CA1 neurons with overlapping place fields distinguished the start and end of trials. At the common starting point of different journeys, the relative spike timing of the neurons was highly correlated. As the rat approached a common goal from different starting points, however, temporal firing patterns were strongly modulated across journeys even if the cells fired in the same spatial locations within fields, implying that different processes influenced when and where cells fire. Spike timing within hippocampal ensembles may thereby help parse the beginning from the end of episodes in memory.

Action Potentials↗

Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity.

The immediate-early gene (IEG) Arc is transcribed after behavioral and physiological treatments that induce synaptic plasticity and is implicated in memory consolidation. The relative contributions of neuronal activity and learning-related plasticity to the behavioral induction of Arc remain to be defined. To differentiate the contributions of each, we assessed the induction of Arc transcription in rats with fornix lesions that impair hippocampal learning yet leave cortical connectivity and neuronal firing essentially intact. Arc expression was assessed after exploration of novel environments and performance of a novel water maze task during which normal rats learned the spatial location of an escape platform. During the same task, rats with fornix lesions learned to approach a visible platform but did not learn its spatial location. Rats with fornix lesions had normal baseline levels of hippocampal Arc mRNA, but unlike normal rats, expression was not increased in response to water maze training. The integrity of signaling pathways controlling Arc expression was demonstrated by stimulation of the medial perforant path, which induced normal synaptic potentiation and Arc in rats with fornix lesions. Together, the results demonstrate that Arc induction can be decoupled from behavior and is more likely to indicate the engagement of synaptic plasticity mechanisms than synaptic or neuronal activity per se. The results further imply that fornix lesions may impair memory in part by decoupling neuronal activity from signaling pathways required for long-lasting hippocampal synaptic plasticity.

Animals↗

Episodic memory--from brain to mind.

Neuronal mechanisms of episodic memory, the conscious recollection of autobiographical events, are largely unknown because electrophysiological studies in humans are conducted only in exceptional circumstances. Unit recording studies in animals are thus crucial for understanding the neurophysiological substrate that enables people to remember their individual past. Two features of episodic memory--autonoetic consciousness, the self-aware ability to "travel through time", and one-trial learning, the acquisition of information in one occurrence of the event--raise important questions about the validity of animal models and the ability of unit recording studies to capture essential aspects of memory for episodes. We argue that autonoetic experience is a feature of human consciousness rather than an obligatory aspect of memory for episodes, and that episodic memory is reconstructive and thus its key features can be modeled in animal behavioral tasks that do not involve either autonoetic consciousness or one-trial learning. We propose that the most powerful strategy for investigating neurophysiological mechanisms of episodic memory entails recording unit activity in brain areas homologous to those required for episodic memory in humans (e.g., hippocampus and prefrontal cortex) as animals perform tasks with explicitly defined episodic-like aspects. Within this framework, empirical data suggest that the basic structure of episodic memory is a temporally extended representation that distinguishes the beginning from the end of an event. Future research is needed to fully understand how neural encodings of context, sequences of items/events, and goals are integrated within mnemonic representations of autobiographical events.

Action Potentials↗

Retrieving memories via internal context requires the hippocampus.

Episodic memory encodes the unique contexts of events so that people can remember the details of an experience when cued by only a subset of event features (Tulving, 1972). In humans, the hippocampus is crucial for this kind of memory (Scoville and Milner, 1957; Vargha-Khadem et al., 1997). The present study tested whether the hippocampus was required for nonspatial, context-dependent memory retrieval in rats that were trained in a constant external environment to approach different nonspatial goal objects depending on their current internal motivational state (hunger or thirst). The rats learned to reliably approach the correct goal and thus used internal context to guide associative memory retrieval. Both fornix transection and selective neurotoxic hippocampal lesions severely impaired memory performance, but cue and motivational discrimination, as well as stimulus-reward associations, were preserved. The findings suggest that the hippocampus is required for using internal contextual information for flexible associative memory retrieval.

Animals↗

Prospective and retrospective memory coding in the hippocampus.

The effect of memory on hippocampal neuronal activity was assessed as rats performed a spatial task that was impaired by fornix lesions. The influences of current location, recently entered places, and places about to be entered were compared. Three new findings emerged. (1) Current, retrospective, and prospective coding were common and recorded simultaneously in neural ensembles. (2) The origin of journeys influenced firing even when rats made detours, showing that recent memory could modulate neuronal activity more than spatial trajectory. (3) Diminished retrospective coding and, more markedly, reduced prospective coding in error trials suggested that the neuronal signal was important for task performance. The population of hippocampal neurons thus encoded information about the recent past, the present, and the imminent future, consistent with a neuronal mechanism for episodic memory.

Animals↗