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Miller, E. K.

Publications and source records attributed to Miller, E. K..

7 recordsLinked to original sources

Intrinsic neuronal dynamics predict distinct functional roles during working memory

Working memory (WM) is characterized by the ability to maintain stable representations over time; however, neural activity associated with WM maintenance can be highly dynamic. We explore whether complex population coding dynamics during WM relate to the intrinsic temporal properties of single neurons in lateral prefrontal cortex (lPFC), the frontal eye fields (FEF) and lateral intraparietal cortex (LIP) of two monkeys (Macaca mulatta). We found that cells with short timescales carried memory information relatively early during memory encoding in lPFC; whereas long timescale cells played a greater role later during processing, dominating coding in the delay period. We also observed a link between functional connectivity at rest and intrinsic timescale in FEF and LIP. Our results indicate that individual differences in the temporal processing capacity predicts complex neuronal dynamics during WM; ranging from rapid dynamic encoding of stimuli to slower, but stable, maintenance of mnemonic information.

neuroscience

Gradual progression from sensory to task-related processing in cerebral cortex

Somewhere along the cortical hierarchy, behaviorally relevant information is distilled from raw sensory inputs. We examined how this transformation progresses along multiple levels of the hierarchy by comparing neural representations in visual, temporal, parietal, and frontal cortices in monkeys categorizing across three visual domains (shape, motion direction, color). Representations in visual areas MT and V4 were tightly linked to external sensory inputs. In contrast, lateral prefrontal cortex (PFC) largely represented the abstracted behavioral relevance of stimuli (task rule, motion category, color category). Intermediate-level areas--posterior inferotemporal (PIT), lateral intraparietal (LIP), and frontal eye fields (FEF)--exhibited mixed representations. While the distribution of sensory information across areas aligned well with classical functional divisions--MT carried stronger motion information, V4 and PIT carried stronger color and shape information--categorical abstraction did not, suggesting these areas may participate in different networks for stimulus-driven and cognitive functions. Paralleling these representational differences, the dimensionality of neural population activity decreased progressively from sensory to intermediate to frontal cortex. This shows how raw sensory representations are transformed into behaviorally relevant abstractions and suggests that the dimensionality of neural activity in higher cortical regions may be specific to their current task.\n\nSignificance statementThe earliest stages of processing in cerebral cortex reflect a relatively faithful copy of sensory inputs, but intelligent behavior requires abstracting behaviorally relevant concepts and categories. We examined how this transformation progresses through multiple levels of the cortical hierarchy by comparing neural representations in six cortical areas in monkeys categorizing across three visual domains. We found that categorical abstraction occurred in a gradual fashion across the cortical hierarchy and reached an apex in prefrontal cortex. Categorical coding did not respect classical models of large-scale cortical organization. The dimensionality of neural population activity was reduced in parallel with these representational changes. Our results shed light on how raw sensory inputs are transformed into behaviorally relevant abstractions.

neuroscience

Working Memory Load Modulates Neuronal Coupling

There is a severe limitation in the number of items that can be held in working memory. However, the neurophysiological limits remain unknown. We asked whether the capacity limit might be explained by differences in neuronal coupling. We developed a theoretical model based on Predictive Coding and used it to analyze Cross Spectral Density data from the prefrontal cortex (PFC), frontal eye fields (FEF) and lateral intraparietal area (LIP). Monkeys performed a change detection task (Buschman et al., 2011). The number of objects that had to be remembered (memory load) was varied (1-3 objects in the same visual hemifield). Changes in memory load changed the connectivity in the PFC-FEF-LIP network. Feedback (top-down) coupling broke down when the number of objects exceeded cognitive capacity. This provides new insights into the neuronal underpinnings of cognitive capacity and how coupling in a distributed working memory network is affected by memory load.

neuroscience

Neuronal rhythms orchestrate cell assembles to distinguish perceptual categories

Categories are reflected in the spiking activity of neurons. However, how neurons form ensembles for categories is unclear. To address this, we simultaneously recorded spiking and local field potential (LFP) activity in the lateral prefrontal cortex (lPFC) of monkeys performing a delayed match to category task with two independent category sets (Animals: Cats vs Dogs; Cars: Sports Cars vs Sedans). We found stimulus and category information in alpha and beta band oscillations. Different category distinctions engaged different frequencies. There was greater spike field coherence (SFC) in alpha ([~]8-14 Hz) for Cats and in beta ([~]16-22 Hz) for Dogs. Cars showed similar differences, albeit less pronounced: greater alpha SFC for Sedans and greater beta SFC for Sports Cars. Thus, oscillatory rhythms can help coordinate neurons into different ensembles. Engagement of different frequencies may help differentiate the categories.

animal behavior and cognition

Hebbian Learning in a Random Network Captures Selectivity Properties of Prefrontal Cortex

Complex cognitive behaviors, such as context-switching and rule-following, are thought to be supported by prefrontal cortex (PFC). Neural activity in PFC must thus be specialized to specific tasks while retaining flexibility. Nonlinear mixed selectivity is an important neurophysiological trait for enabling complex and context-dependent behaviors. Here we investigate (1) the extent to which PFC exhibits computationally relevant properties such as mixed selectivity and (2) how such properties could arise via circuit mechanisms. We show that PFC cells recorded from male and female rhesus macaques during a complex task show a moderate level of specialization and structure that is not replicated by a model wherein cells receive random feedforward inputs. While random connectivity can be effective at generating mixed selectivity, the data shows significantly more mixed selectivity than predicted by a model with otherwise matched parameters. A simple Hebbian learning rule applied to the random connectivity, however, increases mixed selectivity and allows the model to match the data more accurately. To explain how learning achieves this, we provide analysis along with a clear geometric interpretation of the impact of learning on selectivity. After learning, the model also matches the data on measures of noise, response density, clustering, and the distribution of selectivities. Of two styles of Hebbian learning tested, the simpler and more biologically plausible option better matches the data. These modeling results give intuition about how neural properties important for cognition can arise in a circuit and make clear experimental predictions regarding how various measures of selectivity would evolve during animal training.\n\nSignificance StatementPrefrontal cortex (PFC) is a brain region believed to support the ability of animals to engage in complex behavior. How neurons in this area respond to stimuli--and in particular, to combinations of stimuli (\"mixed selectivity\")--is a topic of interest. Despite the fact that models with random feedforward connectivity are capable of creating computationally-relevant mixed selectivity, such a model does not match the levels of mixed selectivity seen in the data analyzed in this study. Adding simple Hebbian learning to the model increases mixed selectivity to the correct level and makes the model match the data on several other relevant measures. This study thus offers predictions on how mixed selectivity and other properties evolve with training.

neuroscience

Compressed timeline of recent experience in monkey lPFC

Cognitive theories suggest that working memory maintains not only the identity of recently-presented stimuli but also a sense of the elapsed time since the stimuli presentation. Previous studies of the neural underpinnings of working memory have focused on sustained firing, which can account for maintenance of the stimulus identity, but not for representation of the elapsed time. We analyzed single-unit recordings from the macaque lateral prefrontal cortex (lPFC) during performance of a delayed-match-to-category task. The sample stimulus triggered a consistent sequence of neurons, each neuron in the sequence firing during a circumscribed period of time. The sequences initiated by different sample stimuli were distinct but overlapping, with the degree of overlap reflecting the visual similarity of the stimuli that caused the sequences. These sequences of neurons encoded both stimulus identity and the elapsed time. The temporal code became less precise as the sample stimulus receded into the past. These findings suggest that working memory is maintained as a compressed timeline, consistent with longstanding cognitive theories of human memory.

neuroscience

Gamma and beta bursts during working memory read-out suggest roles in its volitional control

Working memory (WM) activity is not as stationary or sustained as previously thought. There are brief bursts of gamma ([~]55-120 Hz) and beta ([~]20-35 Hz) oscillations, the former linked to stimulus information in spiking. We examine these dynamics in relation to read-out from WM, which is still not well understood. Monkeys held a sequence of two objects and had to decide if they matched a subsequent sequence. Changes in the balance of beta/gamma suggested their role in WM control. In anticipation of having to use an object for the match decision, there was an increase in spiking information about that object along with an increase in gamma and a decrease in beta. When an object was no longer needed, beta increased and gamma as well as spiking information about that object decreased. Deviations from these dynamics predicted behavioral errors. Thus, turning up or down beta could regulate gamma and the information in working memory.

neuroscience