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Reliable, noninvasive biomarkers that reveal the internal state of a subject are an invaluable tool for neurological diagnoses. Small fixational eye movements, called microsaccades, are a candidate biomarker thought to reflect a subject's focus of attention [Z. M. Hafed, J. J. Clark, VisionRes. 42 , 2533–2545 (2002); R. Engbert, R. Kliegl, VisionRes. 43 , 1035–1045 (2003)]. The linkage between the direction of microsaccades and attention has mainly been demonstrated using explicit and unambiguous attentional cues. However, the natural world is seldom predictable and rarely provides unambiguous information. Thus, a useful biomarker must be robust to such changes in environmental statistics. To determine how well microsaccades reveal visual-spatial attention across behavioral contexts, we analyzed these fixational eye movements in monkeys performing a conventional change detection task. The task included two stimulus locations and variable cue validities across blocks of trials. Subjects were adept at the task, showing precise and graded modulations of visual attention for subtle target changes and performing better and faster when the cue was more reliable [J. P. Mayo, J. H. R. Maunsell, J. Neurosci. 36 , 5353 (2016)]. However, over tens of thousands of microsaccades, we found no difference in microsaccade direction between cued locations when cue variability was high nor between hit and miss trials. Instead, microsaccades were made toward the midpoint of the two target locations, not toward individual targets. Our results suggest that the direction of microsaccades should be interpreted with caution and may not be a reliable measure of covert spatial attention in more complex viewing conditions.

Conventional analysis of neuroscience data involves computing average neural activity over a group of trials and/or a period of time. This approach may be particularly problematic when assessing the response patterns of neurons to more than one simultaneously presented stimulus. In such cases, the brain must represent each individual component of the stimuli bundle, but trial-and-time-pooled averaging methods are fundamentally unequipped to address the means by which multi-item representation occurs. We introduce and investigate a novel statistical analysis framework that relates the firing pattern of a single cell, exposed to a stimuli bundle, to the ensemble of its firing patterns under each constituent stimulus. Existing statistical tools focus on what may be called "first order stochasticity" in trial-to-trial variation in the form of unstructured noise around a fixed firing rate curve associated with a given stimulus. Our analysis is based upon the theoretical premise that exposure to a stimuli bundle induces additional stochasticity in the cell's response pattern, in the form of a stochastically varying recombination of its single stimulus firing rate curves. We discuss challenges to statistical estimation of such "second order stochasticity" and address them with a novel dynamic admixture Poisson process (DAPP) model. DAPP is a hierarchical point process model that decomposes second order stochasticity into a Gaussian stochastic process and a random vector of interpretable features, and, facilitates borrowing of information on the latter across repeated trials through latent clustering. We present empirical evidence of the utility of the DAPP analysis with synthetic and real neural recordings., Comment: 26 pages, 7 figures

How we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One commonly proposed hypothesis is that the sharpness of tuning curves might change to limit the number of stimuli driving any given neuron when multiple stimuli are present. To test this hypothesis, we recorded the activity of neurons in the inferior colliculus while monkeys made saccades to either one or two simultaneous sounds differing in frequency and spatial location. Although monkeys easily distinguished simultaneous sounds (∼90% correct performance), the frequency selectivity of inferior colliculus neurons on dual sound trials did not improve in any obvious way. Frequency selectivity was degraded on dual sound trials compared to single sound trials: neural response functions broadened, and frequency accounted for less of the variance in firing rate. These changes in neural firing led a maximum-likelihood decoder to perform worse on dual sound trials than on single sound trials. These results fail to support the hypothesis that changes in frequency response functions serve to reduce the overlap in the representation of simultaneous sounds. Instead, these results suggest that alternative possibilities, such as recent evidence of alternations in firing rate between the rates corresponding to each of the two stimuli, offer a more promising approach.Graphic AbstractHow sensory representations encode multiple stimuli despite coarse coding is unknown. Using a maximum likelihood decoder operating on the spike count response patterns of monkey inferior colliculus neurons, we show a marked reduction in decoding accuracy when two sounds are presented compared to one. The decoding was inferior to the behavioral performance of the animals, and thus suggests the presence of alternative coding strategies.

Summary The superior colliculus is canonically viewed as a controller of extra-foveal gaze. This traditional view of superior colliculus function is challenged by the discovery that it has an expanded foveal magnification, comparable to that in primary visual cortex.

This chapter reviews the literature on how auditory signals are transformed into a coordinate system that facilitates interactions with the visual system. Sound location is deduced from cues that depend on the position of the sound with respect to the head, but visual location is deduced from the pattern of light illuminating the retina, yielding an eye-centered code. Connecting sights and sounds originating from the same position in the physical world requires the brain to incorporate information about the position of the eyes with respect to the head. Eye position has been found to interact with auditory signals at all levels of the auditory pathway that have been tested but usually yields a code that is in a hybrid reference frame: neither head nor eye centered. Computing a coordinate transformation, in principle, may be easy, which could suggest that the looseness of the computational constraints may permit hybrid coding. A review of the behavioral literature addressing the effects of eye gaze on auditory spatial perception and a discussion of its consistency with physiological observations concludes the chapter.

How the brain preserves information about multiple simultaneous items is poorly understood. We report that single neurons can represent multiple different stimuli by interleaving different signals across time. We record single units in an auditory region, the inferior colliculus, while monkeys localize 1 or 2 simultaneous sounds. During dual-sound trials, we find that some neurons fluctuate between firing rates observed for each single sound, either on a whole-trial or on a sub-trial timescale. These fluctuations are correlated in pairs of neurons, can be predicted by the state of local field potentials prior to sound onset, and, in one monkey, can predict which sound will be reported first. We find corroborating evidence of fluctuating activity patterns in a separate data set involving responses of inferotemporal cortex neurons to multiple visual stimuli. Alternation between activity patterns corresponding to each of multiple items may therefore be a general strategy to enhance the brain processing capacity, potentially linking such disparate phenomena as variable neural firing, neural oscillations, and limits in attentional/memory capacity.

Fearful experiences can produce long-lasting and debilitating memories. Extinction of the fear response requires consolidation of new memories that compete with fearful associations. Subjects with posttraumatic stress disorder (PTSD) show impaired extinction of conditioned fear, which is associated with decreased ventromedial prefrontal cortex (vmPFC) control over amygdala activity. Vagus nerve stimulation (VNS) enhances memory consolidation in both rats and humans, and pairing VNS with exposure to conditioned cues enhances the consolidation of extinction learning in rats. Here we investigated whether pairing VNS with extinction learning facilitates plasticity between the infralimbic (IL) medial prefrontal cortex and the basolateral complex of the amygdala (BLA). Rats were trained on an auditory fear conditioning task, which was followed by a retention test and 1 day of extinction training. Vagus nerve stimulation or sham-stimulation was administered concurrently with exposure to the fear-conditioned stimulus and retention of fear conditioning was tested again 24 h later. Vagus nerve stimulation-treated rats demonstrated a significant reduction in freezing after a single extinction training session similar to animals that received 5× the number of extinction pairings. To study plasticity in the IL-BLA pathway, we recorded evoked field potentials (EFPs) in the BLA in anesthetized animals 24 h after retention testing. Brief burst stimulation in the IL produced LTD in the BLA field response in fear-conditioned and sham-treated animals. In contrast, the same stimulation resulted in potentiation of the IL-BLA pathway in the VNS-treated group. The present findings suggest that VNS promotes plasticity in the IL-BLA pathway to facilitate extinction of conditioned fear responses (CFRs).