Modulating brain oscillations to drive brain function

Do neuronal oscillations play a causal role in brain function? In a study in this issue of PLOS Biology, Helfrich and colleagues address this long-standing question by attempting to drive brain oscillations using transcranial electrical current stimulation. Remarkably, they were able to manipulate visual perception by forcing brain oscillations of the left and right visual hemispheres into synchrony using oscillatory currents over both hemispheres. Under this condition, human observers more often perceived an inherently ambiguous visual stimulus in one of its perceptual instantiations. These findings shed light on the mechanisms underlying neuronal computation. They show that it is the neuronal oscillations that drive the visual experience, not the experience driving the oscillations. And they indicate that synchronized oscillatory activity groups brain areas into functional networks. This points to new ways for controlled experimental and possibly also clinical interventions for the study and modulation of brain oscillations and associated functions

Temporal Dynamics of Decision-Making during Motion Perception in the Visual Cortex

How does the brain make decisions? Speed and accuracy of perceptual decisions covary with certainty in the input, and correlate with the rate of evidence accumulation in parietal and frontal cortical "decision neurons." A biophysically realistic model of interactions within and between Retina/LGN and cortical areas V1, MT, MST, and LIP, gated by basal ganglia, simulates dynamic properties of decision-making in response to ambiguous visual motion stimuli used by Newsome, Shadlen, and colleagues in their neurophysiological experiments. The model clarifies how brain circuits that solve the aperture problem interact with a recurrent competitive network with self-normalizing choice properties to carry out probablistic decisions in real time. Some scientists claim that perception and decision-making can be described using Bayesian inference or related general statistical ideas, that estimate the optimal interpretation of the stimulus given priors and likelihoods. However, such concepts do not propose the neocortical mechanisms that enable perception, and make decisions. The present model explains behavioral and neurophysiological decision-making data without an appeal to Bayesian concepts and, unlike other existing models of these data, generates perceptual representations and choice dynamics in response to the experimental visual stimuli. Quantitative model simulations include the time course of LIP neuronal dynamics, as well as behavioral accuracy and reaction time properties, during both correct and error trials at different levels of input ambiguity in both fixed duration and reaction time tasks. Model MT/MST interactions compute the global direction of random dot motion stimuli, while model LIP computes the stochastic perceptual decision that leads to a saccadic eye movement.National Science Foundation (SBE-0354378, IIS-02-05271); Office of Naval Research (N00014-01-1-0624); National Institutes of Health (R01-DC-02852

Neural Dynamics of Motion Grouping: From Aperture Ambiguity to Object Speed and Direction

A neural network model of visual motion perception and speed discrimination is developed to simulate data concerning the conditions under which components of moving stimuli cohere or not into a global direction of motion, as in barberpole and plaid patterns (both Type 1 and Type 2). The model also simulates how the perceived speed of lines moving in a prescribed direction depends upon their orientation, length, duration, and contrast. Motion direction and speed both emerge as part of an interactive motion grouping or segmentation process. The model proposes a solution to the global aperture problem by showing how information from feature tracking points, namely locations from which unambiguous motion directions can be computed, can propagate to ambiguous motion direction points, and capture the motion signals there. The model does this without computing intersections of constraints or parallel Fourier and non-Fourier pathways. Instead, the model uses orientationally-unselective cell responses to activate directionally-tuned transient cells. These transient cells, in turn, activate spatially short-range filters and competitive mechanisms over multiple spatial scales to generate speed-tuned and directionally-tuned cells. Spatially long-range filters and top-down feedback from grouping cells are then used to track motion of featural points and to select and propagate correct motion directions to ambiguous motion points. Top-down grouping can also prime the system to attend a particular motion direction. The model hereby links low-level automatic motion processing with attention-based motion processing. Homologs of model mechanisms have been used in models of other brain systems to simulate data about visual grouping, figure-ground separation, and speech perception. Earlier versions of the model have simulated data about short-range and long-range apparent motion, second-order motion, and the effects of parvocellular and magnocellular LGN lesions on motion perception.Office of Naval Research (N00014-920J-4015, N00014-91-J-4100, N00014-95-1-0657, N00014-95-1-0409, N00014-91-J-0597); Air Force Office of Scientific Research (F4620-92-J-0225, F49620-92-J-0499); National Science Foundation (IRI-90-00530

What Is Wrong with the No-Report Paradigm and How to Fix It

Is consciousness based in prefrontal circuits involved in cognitive processes like thought, reasoning, and memory or, alternatively, is it based in sensory areas in the back of the neocortex? The no-report paradigm has been crucial to this debate because it aims to separate the neural basis of the cognitive processes underlying post-perceptual decision and report from the neural basis of conscious perception itself. However, the no-report paradigm is problematic because, even in the absence of report, subjects might engage in post-perceptual cognitive processing. Therefore, to isolate the neural basis of consciousness, a no-cognition paradigm is needed. Here, I describe a no-cognition approach to binocular rivalry and outline how this approach can help resolve debates about the neural basis of consciousness

A sensory integration account for time perception

The connection between stimulus perception and time perception remains unknown. The present study combines human and rat psychophysics with sensory cortical neuronal firing to construct a computational model for the percept of elapsed time embedded within sense of touch. When subjects judged the duration of a vibration applied to the fingertip (human) or whiskers (rat), increasing stimulus intensity led to increasing perceived duration. Symmetrically, increasing vibration duration led to increasing perceived intensity. We modeled spike trains from vibrissal somatosensory cortex as input to dual leaky integrators \u2013 an intensity integrator with short time constant and a duration integrator with long time constant \u2013 generating neurometric functions that replicated the actual psychophysical functions of rats. Returning to human psychophysics, we then confirmed specific predictions of the dual leaky integrator model. This study offers a framework, based on sensory coding and subsequent accumulation of sensory drive, to account for how a feeling of the passage of time accompanies the tactile sensory experience

ARSTREAM: A Neural Network Model of Auditory Scene Analysis and Source Segregation

Multiple sound sources often contain harmonics that overlap and may be degraded by environmental noise. The auditory system is capable of teasing apart these sources into distinct mental objects, or streams. Such an "auditory scene analysis" enables the brain to solve the cocktail party problem. A neural network model of auditory scene analysis, called the AIRSTREAM model, is presented to propose how the brain accomplishes this feat. The model clarifies how the frequency components that correspond to a give acoustic source may be coherently grouped together into distinct streams based on pitch and spatial cues. The model also clarifies how multiple streams may be distinguishes and seperated by the brain. Streams are formed as spectral-pitch resonances that emerge through feedback interactions between frequency-specific spectral representaion of a sound source and its pitch. First, the model transforms a sound into a spatial pattern of frequency-specific activation across a spectral stream layer. The sound has multiple parallel representations at this layer. A sound's spectral representation activates a bottom-up filter that is sensitive to harmonics of the sound's pitch. The filter activates a pitch category which, in turn, activate a top-down expectation that allows one voice or instrument to be tracked through a noisy multiple source environment. Spectral components are suppressed if they do not match harmonics of the top-down expectation that is read-out by the selected pitch, thereby allowing another stream to capture these components, as in the "old-plus-new-heuristic" of Bregman. Multiple simultaneously occuring spectral-pitch resonances can hereby emerge. These resonance and matching mechanisms are specialized versions of Adaptive Resonance Theory, or ART, which clarifies how pitch representations can self-organize durin learning of harmonic bottom-up filters and top-down expectations. The model also clarifies how spatial location cues can help to disambiguate two sources with similar spectral cures. Data are simulated from psychophysical grouping experiments, such as how a tone sweeping upwards in frequency creates a bounce percept by grouping with a downward sweeping tone due to proximity in frequency, even if noise replaces the tones at their interection point. Illusory auditory percepts are also simulated, such as the auditory continuity illusion of a tone continuing through a noise burst even if the tone is not present during the noise, and the scale illusion of Deutsch whereby downward and upward scales presented alternately to the two ears are regrouped based on frequency proximity, leading to a bounce percept. Since related sorts of resonances have been used to quantitatively simulate psychophysical data about speech perception, the model strengthens the hypothesis the ART-like mechanisms are used at multiple levels of the auditory system. Proposals for developing the model to explain more complex streaming data are also provided.Air Force Office of Scientific Research (F49620-01-1-0397, F49620-92-J-0225); Office of Naval Research (N00014-01-1-0624); Advanced Research Projects Agency (N00014-92-J-4015); British Petroleum (89A-1204); National Science Foundation (IRI-90-00530); American Society of Engineering Educatio

Cortical Dynamics of Contextually-Cued Attentive Visual Learning and Search: Spatial and Object Evidence Accumulation

How do humans use predictive contextual information to facilitate visual search? How are consistently paired scenic objects and positions learned and used to more efficiently guide search in familiar scenes? For example, a certain combination of objects can define a context for a kitchen and trigger a more efficient search for a typical object, such as a sink, in that context. A neural model, ARTSCENE Search, is developed to illustrate the neural mechanisms of such memory-based contextual learning and guidance, and to explain challenging behavioral data on positive/negative, spatial/object, and local/distant global cueing effects during visual search. The model proposes how global scene layout at a first glance rapidly forms a hypothesis about the target location. This hypothesis is then incrementally refined by enhancing target-like objects in space as a scene is scanned with saccadic eye movements. The model clarifies the functional roles of neuroanatomical, neurophysiological, and neuroimaging data in visual search for a desired goal object. In particular, the model simulates the interactive dynamics of spatial and object contextual cueing in the cortical What and Where streams starting from early visual areas through medial temporal lobe to prefrontal cortex. After learning, model dorsolateral prefrontal cortical cells (area 46) prime possible target locations in posterior parietal cortex based on goalmodulated percepts of spatial scene gist represented in parahippocampal cortex, whereas model ventral prefrontal cortical cells (area 47/12) prime possible target object representations in inferior temporal cortex based on the history of viewed objects represented in perirhinal cortex. The model hereby predicts how the cortical What and Where streams cooperate during scene perception, learning, and memory to accumulate evidence over time to drive efficient visual search of familiar scenes.CELEST, an NSF Science of Learning Center (SBE-0354378); SyNAPSE program of Defense Advanced Research Projects Agency (HR0011-09-3-0001, HR0011-09-C-0011

The Resonant Dynamics of Speech Perception: Interword Integration and Duration-Dependent Backward Effects

How do listeners integrate temporally distributed phonemic information into coherent representations of syllables and words? During fluent speech perception, variations in the durations of speech sounds and silent pauses can produce different pereeived groupings. For exarnple, increasing the silence interval between the words "gray chip" may result in the percept "great chip", whereas increasing the duration of fricative noise in "chip" may alter the percept to "great ship" (Repp et al., 1978). The ARTWORD neural model quantitatively simulates such context-sensitive speech data. In AHTWORD, sequential activation and storage of phonemic items in working memory provides bottom-up input to unitized representations, or list chunks, that group together sequences of items of variable length. The list chunks compete with each other as they dynamically integrate this bottom-up information. The winning groupings feed back to provide top-down supportto their phonemic items. Feedback establishes a resonance which temporarily boosts the activation levels of selected items and chunks, thereby creating an emergent conscious percept. Because the resonance evolves more slowly than wotking memory activation, it can be influenced by information presented after relatively long intervening silence intervals. The same phonemic input can hereby yield different groupings depending on its arrival time. Processes of resonant transfer and competitive teaming help determine which groupings win the competition. Habituating levels of neurotransmitter along the pathways that sustain the resonant feedback lead to a resonant collapsee that permits the formation of subsequent. resonances.Air Force Office of Scientific Research (F49620-92-J-0225); Defense Advanced Research projects Agency and Office of Naval Research (N00014-95-1-0409); National Science Foundation (IRI-97-20333); Office of Naval Research (N00014-92-J-1309, NOOO14-95-1-0657

ARSTREAM: A Neural Network Model of Auditory Scene Analysis and Source Segregation

Multiple sound sources often contain harmonics that overlap and may be degraded by environmental noise. The auditory system is capable of teasing apart these sources into distinct mental objects, or streams. Such an "auditory scene analysis" enables the brain to solve the cocktail party problem. A neural network model of auditory scene analysis, called the AIRSTREAM model, is presented to propose how the brain accomplishes this feat. The model clarifies how the frequency components that correspond to a give acoustic source may be coherently grouped together into distinct streams based on pitch and spatial cues. The model also clarifies how multiple streams may be distinguishes and seperated by the brain. Streams are formed as spectral-pitch resonances that emerge through feedback interactions between frequency-specific spectral representaion of a sound source and its pitch. First, the model transforms a sound into a spatial pattern of frequency-specific activation across a spectral stream layer. The sound has multiple parallel representations at this layer. A sound's spectral representation activates a bottom-up filter that is sensitive to harmonics of the sound's pitch. The filter activates a pitch category which, in turn, activate a top-down expectation that allows one voice or instrument to be tracked through a noisy multiple source environment. Spectral components are suppressed if they do not match harmonics of the top-down expectation that is read-out by the selected pitch, thereby allowing another stream to capture these components, as in the "old-plus-new-heuristic" of Bregman. Multiple simultaneously occuring spectral-pitch resonances can hereby emerge. These resonance and matching mechanisms are specialized versions of Adaptive Resonance Theory, or ART, which clarifies how pitch representations can self-organize durin learning of harmonic bottom-up filters and top-down expectations. The model also clarifies how spatial location cues can help to disambiguate two sources with similar spectral cures. Data are simulated from psychophysical grouping experiments, such as how a tone sweeping upwards in frequency creates a bounce percept by grouping with a downward sweeping tone due to proximity in frequency, even if noise replaces the tones at their interection point. Illusory auditory percepts are also simulated, such as the auditory continuity illusion of a tone continuing through a noise burst even if the tone is not present during the noise, and the scale illusion of Deutsch whereby downward and upward scales presented alternately to the two ears are regrouped based on frequency proximity, leading to a bounce percept. Since related sorts of resonances have been used to quantitatively simulate psychophysical data about speech perception, the model strengthens the hypothesis the ART-like mechanisms are used at multiple levels of the auditory system. Proposals for developing the model to explain more complex streaming data are also provided.Air Force Office of Scientific Research (F49620-01-1-0397, F49620-92-J-0225); Office of Naval Research (N00014-01-1-0624); Advanced Research Projects Agency (N00014-92-J-4015); British Petroleum (89A-1204); National Science Foundation (IRI-90-00530); American Society of Engineering Educatio

Perception of the intensity and duration of a stimulus within a unified framework: psychophysics and underlying neuronal processing

Every sensory experience is embedded in time, and is accompanied by the perception of the passage of time. The fact that perception of the content of a sensory event and the perception of the time occupied by that event are generated in parallel raises a number of questions: Do these percepts interact with each other? Do they emerge within separate neural populations? Which neuronal mechanism underlies this divergence? In the work of my thesis I explored how the perception of the intensity of a vibrotactile stimulus, interacts with the perception of its duration, in both humans and rats. I have carried out three main studies. Chapter I works out the details of the interaction between vibration amplitude and duration, revealing a symmetric confound: perceived duration depends on stimulus speed, and perceived intensity depends on stimulus duration. Quantification of this interaction allowed us formulate a testable computational model for the generation of both percepts, which posits that a single sensory drive provides input to two distinct downstream centers, which generate the two percepts in parallel. Chapter II addresses the effect of stimulus history. Systems neuroscience has given considerable attention in recent years to the effects of preceding stimuli on the perception of the current stimulus. We now ask whether the interaction found in Study I extends to an interaction in the memory trace of recent stimuli: are the perceptual priors mixed or separate? Through psychophysical testing, we were able to show that perception of the duration and the intensity of stimuli, are biased toward the perceived features of previously presented stimuli, and not their low-level physical properties, and that separate representations of prior perceived duration and prior perceived intensity exist in the brain. Chapter III begins to look for neuronal correlates of perceived duration, through extracellular recordings in behaving rats in Dorso-Lateral Striatum (DLS), a region which receives direct input from primary somatosensory cortex and has previously shown to be involved in time perception. The delayed comparison task, differently from many common behavioral paradigms, has the advantage of dissociating the first stimulus presented to the animal from any decisional and motor processes. This makes it particularly relevant for the search for the neural basis of stimulus duration perception. Moreover, the bias of stimulus intensity on perceived time found on Study I, posits the principle that the interaction between these two features should be present in the neural population that encodes the perception of stimulus duration in a behaviourally-relevant way. Ongoing recordings are showing that the unfolding of trial time can be decoded from the striatal neural activity, but the confound of stimulus speed is not encoded by the population. This findings points toward a role of striatum in representing temporal sequences of events, while questioning its involvement in encoding the perception of stimulus duration