Multiple Modes of Phase Locking between Sniffing and Whisking during Active Exploration

Sense organs are often actively controlled by motor processes and such active sensing profoundly shapes the timing of sensory information flow. The temporal coordination between different active sensing processes is less well understood but is essential for multisensory integration, coordination between brain regions, and energetically optimal sampling strategies. Here we studied the coordination between sniffing and whisking, the motor processes in rodents that control the acquisition of smell and touch information, respectively. Sniffing, high-frequency respiratory bouts, and whisking, rapid back and forth movements of mystacial whiskers, occur in the same theta frequency range (4-12 Hz) leading to a hypothesis that these sensorimotor rhythms are phase locked. To test this, we monitored sniffing using a thermocouple in the nasal cavity and whisking with an electromyogram of the mystacial pad in rats engaged in an open field reward foraging behavior. During bouts of exploration, sniffing and whisking showed strong one-to-one phase locking within the theta frequency range (4-12 Hz). Interestingly, we also observed multimode phase locking with multiple whisks within a sniff cycle or multiple sniffs within a whisk cycle-always at the same preferred phase. This specific phase relationship coupled the acquisition phases of the two sensorimotor rhythms, inhalation and whisker protraction. Our results suggest that sniffing and whisking may be under the control of interdependent rhythm generators that dynamically coordinate active acquisition of olfactory and somatosensory information

Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

The basal forebrain (BF) houses major ascending projections to the entire neocortex that have long been implicated in arousal, learning, and attention. The disruption of the BF has been linked with major neurological disorders, such as coma and Alzheimer's disease, as well as in normal cognitive aging. Although it is best known for its cholinergic neurons, the BF is in fact an anatomically and neurochemically complex structure. Recent studies using transgenic mouse lines to target specific BF cell types have led to a renaissance in the study of the BF and are beginning to yield new insights about cell-type-specific circuit mechanisms during behavior. These approaches enable us to determine the behavioral conditions under which cholinergic and noncholinergic BF neurons are activated and how they control cortical processing to influence behavior. Here we discuss recent advances that have expanded our knowledge about this poorly understood brain region and laid the foundation for future cell-type-specific manipulations to modulate arousal, attention, and cortical plasticity in neurological disorders. SIGNIFICANCE STATEMENT: Although the basal forebrain is best known for, and often equated with, acetylcholine-containing neurons that provide most of the cholinergic innervation of the neocortex, it is in fact an anatomically and neurochemically complex structure. Recent studies using transgenic mouse lines to target specific cell types in the basal forebrain have led to a renaissance in this field and are beginning to dissect circuit mechanisms in the basal forebrain during behavior. This review discusses recent advances in the roles of basal forebrain cholinergic and noncholinergic neurons in cognition via their dynamic modulation of cortical activity

Universal features of correlated bursty behaviour

Inhomogeneous temporal processes, like those appearing in human communications, neuron spike trains, and seismic signals, consist of high-activity bursty intervals alternating with long low-activity periods. In recent studies such bursty behavior has been characterized by a fat-tailed inter-event time distribution, while temporal correlations were measured by the autocorrelation function. However, these characteristic functions are not capable to fully characterize temporally correlated heterogenous behavior. Here we show that the distribution of the number of events in a bursty period serves as a good indicator of the dependencies, leading to the universal observation of power-law distribution in a broad class of phenomena. We find that the correlations in these quite different systems can be commonly interpreted by memory effects and described by a simple phenomenological model, which displays temporal behavior qualitatively similar to that in real systems

Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats

Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted multiunit recordings from the SC of rats performing a two-alternative spatial discrimination task using auditory and/or visual stimuli. We found that a large population of SC neurons showed direction-selective activity before the onset of movement in response to the stimuli irrespective of stimulation modality. Trial-by-trial correlation analysis showed that the premovement activity of many SC neurons increased with faster reaction speed for the contraversive movement, whereas the premovement activity of another population of neurons decreased with faster reaction speed for the ipsiversive movement. When visual and auditory stimuli were presented simultaneously, the premovement activity of a population of neurons for the contraversive movement was enhanced, whereas the premovement activity of another population of neurons for the ipsiversive movement was depressed. Unilateral inactivation of SC using muscimol prolonged reaction times of contraversive movements, but it shortened those of ipsiversive movements. These findings suggest that the difference in activity between the SC hemispheres regulates the reaction speed of motor responses, and multisensory information enlarges the activity difference resulting in faster responses

Continuous Evolution of Statistical Estimators for Optimal Decision-Making

In many everyday situations, humans must make precise decisions in the presence of uncertain sensory information. For example, when asked to combine information from multiple sources we often assign greater weight to the more reliable information. It has been proposed that statistical-optimality often observed in human perception and decision-making requires that humans have access to the uncertainty of both their senses and their decisions. However, the mechanisms underlying the processes of uncertainty estimation remain largely unexplored. In this paper we introduce a novel visual tracking experiment that requires subjects to continuously report their evolving perception of the mean and uncertainty of noisy visual cues over time. We show that subjects accumulate sensory information over the course of a trial to form a continuous estimate of the mean, hindered only by natural kinematic constraints (sensorimotor latency etc.). Furthermore, subjects have access to a measure of their continuous objective uncertainty, rapidly acquired from sensory information available within a trial, but limited by natural kinematic constraints and a conservative margin for error. Our results provide the first direct evidence of the continuous mean and uncertainty estimation mechanisms in humans that may underlie optimal decision making

Reshaping of Bulbar Odor Response by Nasal Flow Rate in the Rat

The impact of respiratory dynamics on odor response has been poorly studied at the olfactory bulb level. However, it has been shown that sniffing in the behaving rodent is highly dynamic and varies both in frequency and flow rate. Bulbar odor response could vary with these sniffing parameter variations. Consequently, it is necessary to understand how nasal airflow can modify and shape odor response at the olfactory bulb level.To assess this question, we used a double cannulation and simulated nasal airflow protocol on anesthetized rats to uncouple nasal airflow from animal respiration. Both mitral/tufted cell extracellular unit activity and local field potentials (LFPs) were recorded. We found that airflow changes in the normal range were sufficient to substantially reorganize the response of the olfactory bulb. In particular, cellular odor-evoked activities, LFP oscillations and spike phase-locking to LFPs were strongly modified by nasal flow rate.Our results indicate the importance of reconsidering the notion of odor coding as odor response at the bulbar level is ceaselessly modified by respiratory dynamics

Stable Modality-Specific Activity Flows As Reflected by the Neuroenergetic Approach to the fMRI Weighted Maps

This article uses the ideas of neuroenergetic and neural field theories to detect stimulation-driven energy flows in the brain during face and auditory word processing. In this analysis, energy flows are thought to create the stable gradients of the fMRI weighted summary images. The sources, from which activity spreads in the brain during face processing, were detected in the occipital cortex. The following direction of energy flows in the frontal cortex was described: the right inferior frontal = >the left inferior frontal = >the triangular part of the left inferior frontal cortex = >the left operculum. In the left operculum, a localized circuit was described. For auditory word processing, the sources of activity flows were detected bilaterally in the middle superior temporal regions, they were also detected in the left posterior superior temporal cortex. Thus, neuroenergetic assumptions may give a novel perspective for the analysis of neuroimaging data

Behavioural Correlate of Choice Confidence in a Discrete Trial Paradigm

How animals make choices in a changing and often uncertain environment is a central theme in the behavioural sciences. There is a substantial literature on how animals make choices in various experimental paradigms but less is known about the way they assess a choice after it has been made in terms of the expected outcome. Here, we used a discrete trial paradigm to characterise how the reward history shaped the behaviour on a trial by trial basis. Rats initiated each trial which consisted of a choice between two drinking spouts that differed in their probability of delivering a sucrose solution. Critically, sucrose was delivered after a delay from the first lick at the spouts – this allowed us to characterise the behavioural profile during the window between the time of choice and its outcome. Rats' behaviour converged to optimum choice, both during the acquisition phase and after the reversal of contingencies. We monitored the post-choice behaviour at a temporal precision of 1 millisecond; lick-response profiles revealed that rats spent more time at the spout with the higher reward probability and exhibited a sparser lick pattern. This was the case when we exclusively examined the unrewarded trials, where the outcome was identical. The differential licking profiles preceded the differential choice ratios and could thus predict the changes in choice behaviour

The development of metacognitive ability in adolescence

Introspection, or metacognition, is the capacity to reflect on our own thoughts and behaviours. Here, we investigated how one specific metacognitive ability (the relationship between task performance and confidence) develops in adolescence, a period of life associated with the emergence of self-concept and enhanced self-awareness. We employed a task that dissociates objective performance on a visual task from metacognitive ability in a group of 56 participants aged between 11 and 41 years. Metacognitive ability improved significantly with age during adolescence, was highest in late adolescence and plateaued going into adulthood. Our results suggest that awareness of one’s own perceptual decisions shows a prolonged developmental trajectory during adolescence