A Common Cortical Circuit Mechanism for Perceptual Categorical Discrimination and Veridical Judgment

Perception involves two types of decisions about the sensory world: identification of stimulus features as analog quantities, or discrimination of the same stimulus features among a set of discrete alternatives. Veridical judgment and categorical discrimination have traditionally been conceptualized as two distinct computational problems. Here, we found that these two types of decision making can be subserved by a shared cortical circuit mechanism. We used a continuous recurrent network model to simulate two monkey experiments in which subjects were required to make either a two-alternative forced choice or a veridical judgment about the direction of random-dot motion. The model network is endowed with a continuum of bell-shaped population activity patterns, each representing a possible motion direction. Slow recurrent excitation underlies accumulation of sensory evidence, and its interplay with strong recurrent inhibition leads to decision behaviors. The model reproduced the monkey's performance as well as single-neuron activity in the categorical discrimination task. Furthermore, we examined how direction identification is determined by a combination of sensory stimulation and microstimulation. Using a population-vector measure, we found that direction judgments instantiate winner-take-all (with the population vector coinciding with either the coherent motion direction or the electrically elicited motion direction) when two stimuli are far apart, or vector averaging (with the population vector falling between the two directions) when two stimuli are close to each other. Interestingly, for a broad range of intermediate angular distances between the two stimuli, the network displays a mixed strategy in the sense that direction estimates are stochastically produced by winner-take-all on some trials and by vector averaging on the other trials, a model prediction that is experimentally testable. This work thus lends support to a common neurodynamic framework for both veridical judgment and categorical discrimination in perceptual decision making

Frequency shifts and depth dependence of premotor beta band activity during perceptual decision-making

Neural activity in the premotor and motor cortices shows prominent structure in the beta frequency range (13–30 Hz). Currently, the behavioral relevance of this beta band activity (BBA) is debated. The underlying source of motor BBA and how it changes as a function of cortical depth are also not completely understood. Here, we addressed these unresolved questions by investigating BBA recorded using laminar electrodes in the dorsal premotor cortex of 2 male rhesus macaques performing a visual reaction time (RT) reach discrimination task. We observed robust BBA before and after the onset of the visual stimulus but not during the arm movement. While poststimulus BBA was positively correlated with RT throughout the beta frequency range, prestimulus correlation varied by frequency. Low beta frequencies (∼12–20 Hz) were positively correlated with RT, and high beta frequencies (∼22–30 Hz) were negatively correlated with RT. Analysis and simulations suggested that these frequency-dependent correlations could emerge due to a shift in the component frequencies of the prestimulus BBA as a function of RT, such that faster RTs are accompanied by greater power in high beta frequencies. We also observed a laminar dependence of BBA, with deeper electrodes demonstrating stronger power in low beta frequencies both prestimulus and poststimulus. The heterogeneous nature of BBA and the changing relationship between BBA and RT in different task epochs may be a sign of the differential network dynamics involved in cue expectation, decision-making, motor preparation, and movement execution.Published versio

Distributed functions of prefrontal and parietal cortices during sequential categorical decisions

Comparing sequential stimuli is crucial for guiding complex behaviors. To understand mechanisms underlying sequential decisions, we compared neuronal responses in the prefrontal cortex (PFC), the lateral intraparietal (LIP), and medial intraparietal (MIP) areas in monkeys trained to decide whether sequentially presented stimuli were from matching (M) or nonmatching (NM) categories. We found that PFC leads M/NM decisions, whereas LIP and MIP appear more involved in stimulus evaluation and motor planning, respectively. Compared to LIP, PFC showed greater nonlinear integration of currently visible and remembered stimuli, which correlated with the monkeys’ M/NM decisions. Furthermore, multi-module recurrent networks trained on the same task exhibited key features of PFC and LIP encoding, including nonlinear integration in the PFC-like module, which was causally involved in the networks’ decisions. Network analysis found that nonlinear units have stronger and more widespread connections with input, output, and within-area units, indicating putative circuit-level mechanisms for sequential decisions

Preparing and selecting actions with neural populations: toward cortical circuit mechanisms

How the brain selects one action among multiple alternatives is a central question of neuroscience. An influential model is that action preparation and selection arise from subthreshold activation of the very neurons encoding the action. Recent work, however, shows a much greater diversity of decision-related and action-related signals coexisting with other signals in populations of motor and parietal cortical neurons. We discuss how such distributed signals might be decoded by biologically plausible mechanisms. We also discuss how neurons within cortical circuits might interact with each other during action selection and preparation and how recurrent network models can help to reveal dynamical principles underlying cortical computation.info:eu-repo/semantics/publishedVersio

The Timing of Vision – How Neural Processing Links to Different Temporal Dynamics

In this review, we describe our recent attempts to model the neural correlates of visual perception with biologically inspired networks of spiking neurons, emphasizing the dynamical aspects. Experimental evidence suggests distinct processing modes depending on the type of task the visual system is engaged in. A first mode, crucial for object recognition, deals with rapidly extracting the glimpse of a visual scene in the first 100 ms after its presentation. The promptness of this process points to mainly feedforward processing, which relies on latency coding, and may be shaped by spike timing-dependent plasticity (STDP). Our simulations confirm the plausibility and efficiency of such a scheme. A second mode can be engaged whenever one needs to perform finer perceptual discrimination through evidence accumulation on the order of 400 ms and above. Here, our simulations, together with theoretical considerations, show how predominantly local recurrent connections and long neural time-constants enable the integration and build-up of firing rates on this timescale. In particular, we review how a non-linear model with attractor states induced by strong recurrent connectivity provides straightforward explanations for several recent experimental observations. A third mode, involving additional top-down attentional signals, is relevant for more complex visual scene processing. In the model, as in the brain, these top-down attentional signals shape visual processing by biasing the competition between different pools of neurons. The winning pools may not only have a higher firing rate, but also more synchronous oscillatory activity. This fourth mode, oscillatory activity, leads to faster reaction times and enhanced information transfers in the model. This has indeed been observed experimentally. Moreover, oscillatory activity can format spike times and encode information in the spike phases with respect to the oscillatory cycle. This phenomenon is referred to as “phase-of-firing coding,” and experimental evidence for it is accumulating in the visual system. Simulations show that this code can again be efficiently decoded by STDP. Future work should focus on continuous natural vision, bio-inspired hardware vision systems, and novel experimental paradigms to further distinguish current modeling approaches

Dynamical principles in neuroscience

Dynamical modeling of neural systems and brain functions has a history of success over the last half century. This includes, for example, the explanation and prediction of some features of neural rhythmic behaviors. Many interesting dynamical models of learning and memory based on physiological experiments have been suggested over the last two decades. Dynamical models even of consciousness now exist. Usually these models and results are based on traditional approaches and paradigms of nonlinear dynamics including dynamical chaos. Neural systems are, however, an unusual subject for nonlinear dynamics for several reasons: (i) Even the simplest neural network, with only a few neurons and synaptic connections, has an enormous number of variables and control parameters. These make neural systems adaptive and flexible, and are critical to their biological function. (ii) In contrast to traditional physical systems described by well-known basic principles, first principles governing the dynamics of neural systems are unknown. (iii) Many different neural systems exhibit similar dynamics despite having different architectures and different levels of complexity. (iv) The network architecture and connection strengths are usually not known in detail and therefore the dynamical analysis must, in some sense, be probabilistic. (v) Since nervous systems are able to organize behavior based on sensory inputs, the dynamical modeling of these systems has to explain the transformation of temporal information into combinatorial or combinatorial-temporal codes, and vice versa, for memory and recognition. In this review these problems are discussed in the context of addressing the stimulating questions: What can neuroscience learn from nonlinear dynamics, and what can nonlinear dynamics learn from neuroscience?This work was supported by NSF Grant No. NSF/EIA-0130708, and Grant No. PHY 0414174; NIH Grant No. 1 R01 NS50945 and Grant No. NS40110; MEC BFI2003-07276, and Fundación BBVA

A Cortical Sparse Distributed Coding Model Linking Mini- and Macrocolumn-Scale Functionality

No generic function for the minicolumn – i.e., one that would apply equally well to all cortical areas and species – has yet been proposed. I propose that the minicolumn does have a generic functionality, which only becomes clear when seen in the context of the function of the higher-level, subsuming unit, the macrocolumn. I propose that: (a) a macrocolumn's function is to store sparse distributed representations of its inputs and to be a recognizer of those inputs; and (b) the generic function of the minicolumn is to enforce macrocolumnar code sparseness. The minicolumn, defined here as a physically localized pool of ∼20 L2/3 pyramidals, does this by acting as a winner-take-all (WTA) competitive module, implying that macrocolumnar codes consist of ∼70 active L2/3 cells, assuming ∼70 minicolumns per macrocolumn. I describe an algorithm for activating these codes during both learning and retrievals, which causes more similar inputs to map to more highly intersecting codes, a property which yields ultra-fast (immediate, first-shot) storage and retrieval. The algorithm achieves this by adding an amount of randomness (noise) into the code selection process, which is inversely proportional to an input's familiarity. I propose a possible mapping of the algorithm onto cortical circuitry, and adduce evidence for a neuromodulatory implementation of this familiarity-contingent noise mechanism. The model is distinguished from other recent columnar cortical circuit models in proposing a generic minicolumnar function in which a group of cells within the minicolumn, the L2/3 pyramidals, compete (WTA) to be part of the sparse distributed macrocolumnar code

Optogenetic interrogation of primary visual cortex and its impact on neural coding and behavior

Understanding the mechanism by which the brain transforms simple sensory inputs into rich perceptual experiences is one of the great mysteries of systems neuroscience. Undoubtedly this involves the activity of large populations of interconnected neurons, but while the responses of individual neurons to a variety of sensory stimuli have been well-characterized, how populations of such neurons organize their activity to create our sensory perceptions is almost entirely unknown. To investigate this complex circuitry requires the ability to causally manipulate the activity of neural populations and monitor the resultant effects. Here we focus on primary visual cortex (V1), which has been shown to be crucial for visual perception, and utilize optogenetic tools to render the activity of genetically- defined neural populations sensitive to light. By simultaneously recording and modulating (either driving or silencing) the activity of excitatory (glutamatergic) neurons, we are able to causally examine their role in visual perception. Here we report 3 major findings. First, we show that activating subpopulations of excitatory neurons can improve visual perception under certain conditions and that information in V1 used for perceptual decisions is integrated across spatially-limited populations of neurons. Further, we show that a key signature of this information integration is a reduction in correlated variability between neurons. Correlated variability has been implicated as a major source of behavioral choice related activity in the cortex, and theorized to be a major factor limiting information in cortical populations. However, until now, there has not been a way to manipulate correlations without altering firing rates or other task related variables. Here we demonstrate a novel method using optogenetic stimulation to causally manipulate correlated variability between cortical neurons without altering their firing rates. Lastly, with the goal of expanding the currently limited repertoire of optogenetic tools for non-human primates, we establish the viability of a novel optogenetic construct capable of dramatically silencing neural populations using a recently discovered anion conducting channelrhodopsin

Feed-Forward Propagation of Temporal and Rate Information between Cortical Populations during Coherent Activation in Engineered In Vitro Networks.

Transient propagation of information across neuronal assembles is thought to underlie many cognitive processes. However, the nature of the neural code that is embedded within these transmissions remains uncertain. Much of our understanding of how information is transmitted among these assemblies has been derived from computational models. While these models have been instrumental in understanding these processes they often make simplifying assumptions about the biophysical properties of neurons that may influence the nature and properties expressed. To address this issue we created an in vitro analog of a feed-forward network composed of two small populations (also referred to as assemblies or layers) of living dissociated rat cortical neurons. The populations were separated by, and communicated through, a microelectromechanical systems (MEMS) device containing a strip of microscale tunnels. Delayed culturing of one population in the first layer followed by the second a few days later induced the unidirectional growth of axons through the microtunnels resulting in a primarily feed-forward communication between these two small neural populations. In this study we systematically manipulated the number of tunnels that connected each layer and hence, the number of axons providing communication between those populations. We then assess the effect of reducing the number of tunnels has upon the properties of between-layer communication capacity and fidelity of neural transmission among spike trains transmitted across and within layers. We show evidence based on Victor-Purpura's and van Rossum's spike train similarity metrics supporting the presence of both rate and temporal information embedded within these transmissions whose fidelity increased during communication both between and within layers when the number of tunnels are increased. We also provide evidence reinforcing the role of synchronized activity upon transmission fidelity during the spontaneous synchronized network burst events that propagated between layers and highlight the potential applications of these MEMs devices as a tool for further investigation of structure and functional dynamics among neural populations