Bilinearity, Rules, and Prefrontal Cortex

Humans can be instructed verbally to perform computationally complex cognitive tasks; their performance then improves relatively slowly over the course of practice. Many skills underlie these abilities; in this paper, we focus on the particular question of a uniform architecture for the instantiation of habitual performance and the storage, recall, and execution of simple rules. Our account builds on models of gated working memory, and involves a bilinear architecture for representing conditional input-output maps and for matching rules to the state of the input and working memory. We demonstrate the performance of our model on two paradigmatic tasks used to investigate prefrontal and basal ganglia function

Simple Substrates for Complex Cognition

Complex cognitive tasks present a range of computational and algorithmic challenges for neural accounts of both learning and inference. In particular, it is extremely hard to solve them using the sort of simple policies that have been extensively studied as solutions to elementary Markov decision problems. There has thus been recent interest in architectures for the instantiation and even learning of policies that are formally more complicated than these, involving operations such as gated working memory. However, the focus of these ideas and methods has largely been on what might best be considered as automatized, routine or, in the sense of animal conditioning, habitual, performance. Thus, they have yet to provide a route towards understanding the workings of rule-based control, which is critical for cognitively sophisticated competence. Here, we review a recent suggestion for a uniform architecture for habitual and rule-based execution, discuss some of the habitual mechanisms that underpin the use of rules, and consider a statistical relationship between rules and habits

Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning

Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations. © 2020 National Academy of Sciences. All rights reserved

Synthesizing cognition in neuromorphic electronic systems

The quest to implement intelligent processing in electronic neuromorphic systems lacks methods for achieving reliable behavioral dynamics on substrates of inherently imprecise and noisy neurons. Here we report a solution to this problem that involves first mapping an unreliable hardware layer of spiking silicon neurons into an abstract computational layer composed of generic reliable subnetworks of model neurons and then composing the target behavioral dynamics as a “soft state machine” running on these reliable subnets. In the first step, the neural networks of the abstract layer are realized on the hardware substrate by mapping the neuron circuit bias voltages to the model parameters. This mapping is obtained by an automatic method in which the electronic circuit biases are calibrated against the model parameters by a series of population activity measurements. The abstract computational layer is formed by configuring neural networks as generic soft winner-take-all subnetworks that provide reliable processing by virtue of their active gain, signal restoration, and multistability. The necessary states and transitions of the desired high-level behavior are then easily embedded in the computational layer by introducing only sparse connections between some neurons of the various subnets. We demonstrate this synthesis method for a neuromorphic sensory agent that performs real-time context-dependent classification of motion patterns observed by a silicon retina

Working memory updating and the development of rule-guided behavior

a b s t r a c t The transition from middle childhood into adolescence is marked by both increasing independence and also extensive change in the daily requirements of familial demands, social pressures, and academic achievement. To manage this increased complexity, children must develop the ability to use abstract rules that guide the choice of behavior across a range of circumstances. Here, we tested children through adults in a task that requires increasing levels of rule abstraction, while separately manipulating competition among alternatives in working memory. We found that age-related differences in rule-guided behavior can be explained in terms of improvement in rule abstraction, which we suggest involves a working memory updating mechanism. Furthermore, family socioeconomic status (SES) predicted change in rule-guided behavior, such that higher SES predicted better performance with development. We discuss these results within a working memory gating framework for abstract rule-guided behavior

Multitasking versus multiplexing: Toward a normative account of limitations in the simultaneous execution of control-demanding behaviors

Why is it that behaviors that rely on control, so striking in their diversity and flexibility, are also subject to such striking limitations? Typically, people cannot engage in more than a few—and usually only a single—control-demanding task at a time. This limitation was a defining element in the earliest conceptualizations of controlled processing; it remains one of the most widely accepted axioms of cognitive psychology, and is even the basis for some laws (e.g., against the use of mobile devices while driving). Remarkably, however, the source of this limitation is still not understood. Here, we examine one potential source of this limitation, in terms of a trade-off between the flexibility and efficiency of representation (“multiplexing”) and the simultaneous engagement of different processing pathways (“multitasking”). We show that even a modest amount of multiplexing rapidly introduces cross-talk among processing pathways, thereby constraining the number that can be productively engaged at once. We propose that, given the large number of advantages of efficient coding, the human brain has favored this over the capacity for multitasking of control-demanding processes.National Science Foundation (U.S.). Graduate Research Fellowship Progra

Internal Representation of Task Rules by Recurrent Dynamics: The Importance of the Diversity of Neural Responses

Neural activity of behaving animals, especially in the prefrontal cortex, is highly heterogeneous, with selective responses to diverse aspects of the executed task. We propose a general model of recurrent neural networks that perform complex rule-based tasks, and we show that the diversity of neuronal responses plays a fundamental role when the behavioral responses are context-dependent. Specifically, we found that when the inner mental states encoding the task rules are represented by stable patterns of neural activity (attractors of the neural dynamics), the neurons must be selective for combinations of sensory stimuli and inner mental states. Such mixed selectivity is easily obtained by neurons that connect with random synaptic strengths both to the recurrent network and to neurons encoding sensory inputs. The number of randomly connected neurons needed to solve a task is on average only three times as large as the number of neurons needed in a network designed ad hoc. Moreover, the number of needed neurons grows only linearly with the number of task-relevant events and mental states, provided that each neuron responds to a large proportion of events (dense/distributed coding). A biologically realistic implementation of the model captures several aspects of the activity recorded from monkeys performing context-dependent tasks. Our findings explain the importance of the diversity of neural responses and provide us with simple and general principles for designing attractor neural networks that perform complex computation

Behavioral Signatures of Memory Resources for Language:Looking beyond the Lexicon/Grammar Divide

Although there is a broad consensus that both the procedural and declarative memory systems play a crucial role in language learning, use, and knowledge, the mapping between linguistic types and memory structures remains underspecified: by default, a dual‐route mapping of language systems to memory systems is assumed, with declarative memory handling idiosyncratic lexical knowledge and procedural memory handling rule‐governed knowledge of grammar. We experimentally contrast the processing of morphology (case and aspect), syntax (subordination), and lexical semantics (collocations) in a healthy L1 population of Polish, a language rich in form distinctions. We study the processing of these four types under two conditions: a single task condition in which the grammaticality of stimuli was judged and a concurrent task condition in which grammaticality judgments were combined with a digit span task. Dividing attention impedes access to declarative memory while leaving procedural memory unaffected and hence constitutes a test that dissociates which types of linguistic information each long‐term memory construct subserves. Our findings confirm the existence of a distinction between lexicon and grammar as a generative, dual‐route model would predict, but the distinction is graded, as usage‐based models assume: the hypothesized grammar–lexicon opposition appears as a continuum on which grammatical phenomena can be placed as being more or less “ruly” or “idiosyncratic.” However, usage‐based models, too, need adjusting as not all types of linguistic knowledge are proceduralized to the same extent. This move away from a simple dichotomy fundamentally changes how we think about memory for language, and hence how we design and interpret behavioral and neuroimaging studies that probe into the nature of language cognition

Prefrontal rhythms for cognitive control

Goal-directed behavior requires flexible selection among action plans and updating behavioral strategies when they fail to achieve desired goals. Lateral prefrontal cortex (LPFC) is implicated in the execution of behavior-guiding rule-based cognitive control while anterior cingulate cortex (ACC) is implicated in monitoring processes and updating rules. Rule-based cognitive control requires selective processing while process monitoring benefits from combinatorial processing. I used a combination of computational and experimental methods to investigate how network oscillations and neuronal heterogeneity contribute to cognitive control through their effects on selective versus combinatorial processing modes in LPFC and ACC. First, I adapted an existing LPFC model to explore input frequency- and coherence-based output selection mechanisms for flexible routing of rate-coded signals. I show that the oscillatory states of input encoding populations can exhibit a stronger influence over downstream competition than their activity levels. This enables an output driven by a weaker resonant input signal to suppress lower-frequency competing responses to stronger, less resonant (though possibly higher-frequency) input signals. While signals are encoded in population firing rates, output selection and signal routing can be governed independently by the frequency and coherence of oscillatory inputs and their correspondence with output resonant properties. Flexible response selection and gating can be achieved by oscillatory state control mechanisms operating on input encoding populations. These dynamic mechanisms enable experimentally-observed LPFC beta and gamma oscillations to flexibly govern the selection and gating of rate-coded signals for downstream read-out. Furthermore, I demonstrate how differential drives to distinct interneuron populations can switch working memory representations between asynchronous and oscillatory states that support rule-based selection. Next, I analyzed physiological data from the LeBeau laboratory and built a de novo model constrained by the biological data. Experimental data demonstrated that fast network oscillations at both the beta- and gamma frequency bands could be elicited in vitro in ACC and neurons exhibited a wide range of intrinsic properties. Computational modeling of the ACC network revealed that the frequency of network oscillation generated was dependent upon the time course of inhibition. Principal cell heterogeneity broadened the range of frequencies generated by the model network. In addition, with different frequency inputs to two neuronal assemblies, heterogeneity decreased competition and increased spike coherence between the networks thus conferring a combinatorial advantage to the network. These findings suggest that oscillating neuronal populations can support either response selection (routing), or combination, depending on the interplay between the kinetics of synaptic inhibition and the degree of heterogeneity of principal cell intrinsic conductances. Such differences may support functional differences between the roles of LPFC and ACC in cognitive control