Dynamics of Temporal Integration in the Lateral Geniculate Nucleus.

Before visual information from the retina reaches primary visual cortex (V1), it is dynamically filtered by the lateral geniculate nucleus (LGN) of the thalamus, the first location within the visual hierarchy at which nonretinal structures can significantly influence visual processing. To explore the form and dynamics of geniculate filtering we used data from monosynpatically connected pairs of retinal ganglion cells (RGCs) and LGN relay cells in the cat that, under anesthetized conditions, were stimulated with binary white noise and/or drifting sine-wave gratings to train models of increasing complexity to predict which RGC spikes were relayed to cortex, what we call "relay status." In addition, we analyze and compare a smaller dataset recorded in the awake state to assess how anesthesia might influence our results. Consistent with previous work, we find that the preceding retinal interspike interval (ISI) is the primary determinate of relay status with only modest contributions from longer patterns of retinal spikes. Including the prior activity of the LGN cell further improved model predictions, primarily by indicating epochs of geniculate burst activity in recordings made under anesthesia, and by allowing the model to capture gain control-like behavior within the awake LGN. Using the same modeling framework, we further demonstrate that the form of geniculate filtering changes according to the level of activity within the early visual circuit under certain stimulus conditions. This finding suggests a candidate mechanism by which a stimulus specific form of gain control may operate within the LGN.

The Groove Enhancement Machine (GEM): A Multi-Person Adaptive Metronome to Manipulate Sensorimotor Synchronization and Subjective Enjoyment.

Synchronization of movement enhances cooperation and trust between people. However, the degree to which individuals can synchronize with each other depends on their ability to perceive the timing of others' actions and produce movements accordingly. Here, we introduce an assistive device-a multi-person adaptive metronome-to facilitate synchronization abilities. The adaptive metronome is implemented on Arduino Uno circuit boards, allowing for negligible temporal latency between tapper input and adaptive sonic output. Across five experiments-two single-tapper, and three group (four tapper) experiments, we analyzed the effects of metronome adaptivity (percent correction based on the immediately preceding tap-metronome asynchrony) and auditory feedback on tapping performance and subjective ratings. In all experiments, tapper synchronization with the metronome was significantly enhanced with 25-50% adaptivity, compared to no adaptation. In group experiments with auditory feedback, synchrony remained enhanced even at 70-100% adaptivity; without feedback, synchrony at these high adaptivity levels returned to near baseline. Subjective ratings of being in the groove, in synchrony with the metronome, in synchrony with others, liking the task, and difficulty all reduced to one latent factor, which we termed enjoyment. This same factor structure replicated across all experiments. In predicting enjoyment, we found an interaction between auditory feedback and metronome adaptivity, with increased enjoyment at optimal levels of adaptivity only with auditory feedback and a severe decrease in enjoyment at higher levels of adaptivity, especially without feedback. Exploratory analyses relating person-level variables to tapping performance showed that musical sophistication and trait sadness contributed to the degree to which an individual differed in tapping stability from the group. Nonetheless, individuals and groups benefitted from adaptivity, regardless of their musical sophistication. Further, individuals who tapped less variably than the group (which only occurred ∼25% of the time) were more likely to feel "in the groove." Overall, this work replicates previous single person adaptive metronome studies and extends them to group contexts, thereby contributing to our understanding of the temporal, auditory, psychological, and personal factors underlying interpersonal synchrony and subjective enjoyment during sensorimotor interaction. Further, it provides an open-source tool for studying such factors in a controlled way.

The Augmentation of Retinogeniculate Communication during Thalamic Burst Mode.

Retinal signals are transmitted to cortex via neurons in the lateral geniculate nucleus (LGN), where they are processed in burst or tonic response mode. Burst mode occurs when LGN neurons are sufficiently hyperpolarized for T-type Ca2+ channels to deinactivate, allowing them to open in response to depolarization, which can trigger a high-frequency sequence of Na+-based spikes (i.e., burst). In contrast, T-type channels are inactivated during tonic mode and do not contribute to spiking. Although burst mode is commonly associated with sleep and the disruption of retinogeniculate communication, bursts can also be triggered by visual stimulation, thereby transforming the retinal signals relayed to the cortex. To determine how burst mode affects retinogeniculate communication, we made recordings from monosynaptically connected retinal ganglion cells and LGN neurons in male/female cats during visual stimulation. Our results reveal a robust augmentation of retinal signals within the LGN during burst mode. Specifically, retinal spikes were more effective and often triggered multiple LGN spikes during periods likely to have increased T-type Ca2+ channel activity. Consistent with the biophysical properties of T-type Ca2+ channels, analysis revealed that effect magnitude was correlated with the duration of the preceding thalamic interspike interval and occurred even in the absence of classically defined bursts. Importantly, the augmentation of geniculate responses to retinal input was not associated with a degradation of visual signals. Together, these results indicate a graded nature of response mode and suggest that, under certain conditions, bursts facilitate the transmission of visual information to the cortex by amplifying retinal signals.SIGNIFICANCE STATEMENT The thalamus is the gateway for retinal information traveling to the cortex. The lateral geniculate nucleus, like all thalamic nuclei, has two classically defined categories of spikes-tonic and burst-that differ in their underlying cellular mechanisms. Here we compare retinogeniculate communication during burst and tonic response modes. Our results show that retinogeniculate communication is enhanced during burst mode and visually evoked thalamic bursts, thereby augmenting retinal signals transmitted to cortex. Further, our results demonstrate that the influence of burst mode on retinogeniculate communication is graded and can be measured even in the absence of classically defined thalamic bursts.

Contrast gain control and retinogeniculate communication.

Visual information processed in the retina is transmitted to primary visual cortex via relay cells in the lateral geniculate nucleus (LGN) of the dorsal thalamus. Although retinal ganglion cells are the primary source of driving input to LGN neurons, not all retinal spikes are transmitted to the cortex. Here, we investigate the relationship between stimulus contrast and retinogeniculate communication and test the hypothesis that both the time course and strength of retinogeniculate interactions are dynamic and dependent on stimulus contrast. By simultaneously recording the spiking activity of synaptically connected retinal ganglion cells and LGN neurons in the cat, we show that the temporal window for retinogeniculate integration and the effectiveness of individual retinal spikes are inversely proportional to stimulus contrast. This finding provides a mechanistic understanding for the phenomenon of augmented contrast gain control in the LGN-a nonlinear receptive field property of LGN neurons whereby response gain during low-contrast stimulation is enhanced relative to response gain during high-contrast stimulation. In addition, these results support the view that network interactions beyond the retina play an essential role in transforming visual signals en route from retina to cortex.

Fundamentally Distributed Information Processing Integrates the Motor Network into the Mental Workspace during Mental Rotation.

The manipulation of mental representations in the human brain appears to share similarities with the physical manipulation of real-world objects. In particular, some neuroimaging studies have found increased activity in motor regions during mental rotation, suggesting that mental and physical operations may involve overlapping neural populations. Does the motor network contribute information processing to mental rotation? If so, does it play a similar computational role in both mental and manual rotation, and how does it communicate with the wider network of areas involved in the mental workspace? Here we used multivariate methods and fMRI to study 24 participants as they mentally rotated 3-D objects or manually rotated their hands in one of four directions. We find that information processing related to mental rotations is distributed widely among many cortical and subcortical regions, that the motor network becomes tightly integrated into a wider mental workspace network during mental rotation, and that motor network activity during mental rotation only partially resembles that involved in manual rotation. Additionally, these findings provide evidence that the mental workspace is organized as a distributed core network that dynamically recruits specialized subnetworks for specific tasks as needed.

Information Processing in the Mental Workspace Is Fundamentally Distributed.

The brain is a complex, interconnected information processing network. In humans, this network supports a mental workspace that enables high-level abilities such as scientific and artistic creativity. Do the component processes underlying these abilities occur in discrete anatomical modules, or are they distributed widely throughout the brain? How does the flow of information within this network support specific cognitive functions? Current approaches have limited ability to answer such questions. Here, we report novel multivariate methods to analyze information flow within the mental workspace during visual imagery manipulation. We find that mental imagery entails distributed information flow and shared representations throughout the cortex. These findings challenge existing, anatomically modular models of the neural basis of higher-order mental functions, suggesting that such processes may occur at least in part at a fundamentally distributed level of organization. The novel methods we report may be useful in studying other similarly complex, high-level informational processes.

Readiness potentials driven by non-motoric processes.

An increase in brain activity known as the "readiness potential" (RP) can be seen over central scalp locations in the seconds leading up to a volitionally timed movement. This activity precedes awareness of the ensuing movement by as much as two seconds and has been hypothesized to reflect preconscious planning and/or preparation of the movement. Using a novel experimental design, we teased apart the relative contribution of motor-related and non-motor-related processes to the RP. The results of our experiment reveal that robust RPs occured in the absence of movement and that motor-related processes did not significantly modulate the RP. This suggests that the RP measured here is unlikely to reflect preconscious motor planning or preparation of an ensuing movement, and instead may reflect decision-related or anticipatory processes that are non-motoric in nature.

Hypnotizing Libet: Readiness potentials with non-conscious volition.

The readiness potential (RP) is one of the most controversial topics in neuroscience and philosophy due to its perceived relevance to the role of conscious willing in action. Libet and colleagues reported that RP onset precedes both volitional movement and conscious awareness of willing that movement, suggesting that the experience of conscious will may not cause volitional movement (Libet, Gleason, Wright, & Pearl, 1983). Rather, they suggested that the RP indexes unconscious processes that may actually cause both volitional movement and the accompanying conscious feeling of will (Libet et al., 1983; pg. 640). Here, we demonstrate that volitional movement can occur without an accompanying feeling of will. We additionally show that the neural processes indexed by RPs are insufficient to cause the experience of conscious willing. Specifically, RPs still occur when subjects make self-timed, endogenously-initiated movements due to a post-hypnotic suggestion, without a conscious feeling of having willed those movements.

The artist emerges: visual art learning alters neural structure and function.

How does the brain mediate visual artistic creativity? Here we studied behavioral and neural changes in drawing and painting students compared to students who did not study art. We investigated three aspects of cognition vital to many visual artists: creative cognition, perception, and perception-to-action. We found that the art students became more creative via the reorganization of prefrontal white matter but did not find any significant changes in perceptual ability or related neural activity in the art students relative to the control group. Moreover, the art students improved in their ability to sketch human figures from observation, and multivariate patterns of cortical and cerebellar activity evoked by this drawing task became increasingly separable between art and non-art students. Our findings suggest that the emergence of visual artistic skills is supported by plasticity in neural pathways that enable creative cognition and mediate perceptuomotor integration.

Network structure and dynamics of the mental workspace.

The conscious manipulation of mental representations is central to many creative and uniquely human abilities. How does the human brain mediate such flexible mental operations? Here, multivariate pattern analysis of functional MRI data reveals a widespread neural network that performs specific mental manipulations on the contents of visual imagery. Evolving patterns of neural activity within this mental workspace track the sequence of informational transformations carried out by these manipulations. The network switches between distinct connectivity profiles as representations are maintained or manipulated.

Barking up the wrong free: readiness potentials reflect processes independent of conscious will.

In the early 1980s, Libet found that a readiness potential (RP) over central scalp locations begins on average several hundred milliseconds before the reported time of awareness of willing to move (W). Haggard and Eimer Exp Brain Res 126(1):128-133, (1999) later found no correlation between the timing of the RP and W, suggesting that the RP does not reflect processes causal of W. However, they did find a positive correlation between the onset of the lateralized readiness potential (LRP) and W, suggesting that the LRP might reflect processes causal of W. Here, we report a failure to replicate Haggard and Eimer's LRP finding with a larger group of participants and several variations of their analytical method. Although we did find a between-subject correlation in just one of 12 related analyses of the LRP, we crucially found no within-subject covariation between LRP onset and W. These results suggest that the RP and LRP reflect processes independent of will and consciousness. This conclusion has significant implications for our understanding of the neural basis of motor action and potentially for arguments about free will and the causal role of consciousness.