A Normalization Model of Attentional Modulation of Single Unit Responses

Although many studies have shown that attention to a stimulus can enhance the responses of individual cortical sensory neurons, little is known about how attention accomplishes this change in response. Here, we propose that attention-based changes in neuronal responses depend on the same response normalization mechanism that adjusts sensory responses whenever multiple stimuli are present. We have implemented a model of attention that assumes that attention works only through this normalization mechanism, and show that it can replicate key effects of attention. The model successfully explains how attention changes the gain of responses to individual stimuli and also why modulation by attention is more robust and not a simple gain change when multiple stimuli are present inside a neuron''s receptive field. Additionally, the model accounts well for physiological data that measure separately attentional modulation and sensory normalization of the responses of individual neurons in area MT in visual cortex. The proposal that attention works through a normalization mechanism sheds new light a broad range of observations on how attention alters the representation of sensory information in cerebral cortex.     

High stimulus specificity characterizes anti-predator habituation under natural conditions

Habituation is one of the most fundamental learning processes that allow animals to adapt to dynamic environments. It is ubiquitous and often thought of as a simple form of non-associative learning. Very little is known, though, about the rules that govern habituation and their significance under natural conditions. Questions about how animals incorporate habituation into their daily behaviour and how they can assure only to habituate to non-relevant stimuli are still unanswered. Animals under threat of predation should be particularly selective about which stimuli they habituate to, since ignoring a real threat could be fatal. In this study, we tested the response of fiddler crabs, Uca vomeris, to repeatedly approaching dummy predators to find out whether these animals habituate to potential predators and to test the selectivity of the habituation process. The crabs habituated to model predators, even though they were confronted with real predators during the same habituation process. They showed remarkable selectivity towards the stimulus: a simple change in the approach distance of the stimulus led to a recovery in their responses. The results strongly indicate that in the context of predator avoidance, habituation under natural conditions is highly selective and a stimulus is not defined just by its current sensory signature, but also its spatio-temporal history.     

Fast habituation of the long-latency auditory evoked potential in the awake albino rat

Fast habituation of the long-latency, vertex-recorded auditory evoked potential (AEP) peaks in humans was first described by Callaway (1973) as a reduction in AEP amplitude that occurs to the second of a pair of acoustic stimuli when both stimuli are presented with an interstimulus interval (ISI) of no more than 10 sec. When acoustic stimuli are presented in pairs with an ISI of 2 sec and an interpair interval (IPI) of approximately 10 sec, reduction in amplitude to the second tone occurs by as much as 30–50%. Fast habituation may depend somewhat on a subject's anticipation of the stimulus and on other factors related to attention and orienting. Studies in our laboratory have demonstrated this amplitude decrement to the second tone of a pair in human infants, children and adults and have explored the implications of this finding with respect to attentional processes and the allocation of cerebral resources. In the present investigation we describe an animal model of fast habituation. Here, vertex-recorded AEPs were obtained to paired tone stimuli delivered to awake adult male Sprague-Dawley rats chronically implanted with skull electrodes. Findings showed: (a) an AEP wave form with 8 distinct peaks, (b) for one component there was a marked decrement in amplitude from tone 1 to tone 2 in recordings obtained from an electrode placed slightly to the right of midline, and (c) that there were no significant differences in peak latencies across tones. This methodology may further our understanding of fast habituation in humans and may prove useful for studies of attention, orienting, and resource allocation using techniques that are not possible for use with human subjects.     

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.     

Towards a functional neuroanatomy of conscious perception and its modulation by volition: implications of human auditory neuroimaging studies.

Conscious sensory perception and its modulation by volition are integral to human mental life. Functional neuroimaging techniques provide a direct means of identifying and characterizing in vivo the systems-level patterns of brain activity associated with such mental functions. In a series of positron emission tomography activation experiments, we and our colleagues have examined a range of normal and abnormal auditory states that, when contrasted, provide dissociations relevant to the question of the neural substrates of sensory awareness. These dissociations include sensory awareness in the presence and absence of external sensory stimuli, the transition from sensory unawareness to awareness (or vice versa) in the presence of sensory stimuli, and sensory awareness with and without volition. The auditory states studied include hallucinations, mental imagery, cortical deafness modulated by attention, and hearing modulated by sedation. The results of these studies highlight the distributed nature of the functional neuroanatomy that is sufficient, if not necessary, for sensory awareness. The probable roles of unimodal association (as compared with primary) cortices, heteromodal cortices, limbic/paralimbic regions and subcortical structures (such as the thalamus) are discussed. In addition, interactions between pre- and post-rolandic regions are examined in the context of top-down, volitional modulation of sensory awareness.     

Effect of sectioning the mammillothalamic tract on neurons of limbic nuclei of the thalamus

Neuronal activity of n. AV (n = 75) and n. AD (n = 55) of the thalamus was recorded extracellularly in unanaesthetized chronic rabbits after complete transection of the mammillo -thalamic tract (MTT). Elimination of this powerful afferent system produced a surprisingly small effect upon spontaneous and evoked neuronal activity. All types of responses were preserved in both nuclei, though some increase of multimodal diffuse tonic responses and decrease of more specialized phasic and complex on-effects occurred in n. AV. In both nuclei short-latency responses (less than 14 ms) to auditory stimuli disappeared. The number of units with dynamic transformations of responses during repeated stimuli application (gradual emergence and shaping of responses, as well as their habituation) decreased 2-3-fold in both nuclei. The impulse activity travelling in MTT seems to be not critical for limbic nuclei sensory reactivity but significant for plasticity of the responses.     

Increased Neural Habituation in the Amygdala and Orbitofrontal Cortex in Social Anxiety Disorder Revealed by fMRI

A characterizing symptom of social anxiety disorder (SAD) is increased emotional reactivity towards potential social threat in combination with impaired emotion and stress regulation. While several neuroimaging studies have linked SAD with hyperreactivity in limbic brain regions when exposed to emotional faces, little is known about habituation in both the amygdala and neocortical regulation areas. 15 untreated SAD patients and 15 age- and gender-matched healthy controls underwent functional magnetic resonance imaging during repeated blocks of facial emotion () and object discrimination tasks (). Emotion processing networks were defined by a task-related contrast (). Linear regression was employed for assessing habituation effects in these regions. In both groups, the employed paradigm robustly activated the emotion processing and regulation network, including the amygdalae and orbitofrontal cortex (OFC). Statistically significant habituation effects were found in the amygdalae, OFC, and pulvinar thalamus of SAD patients. No such habituation was found in healthy controls. Concurrent habituation in the medial OFC and the amygdalae of SAD patients as shown in this study suggests intact functional integrity and successful short-term down-regulation of neural activation in brain areas responsible for emotion processing. Initial hyperactivation may be explained by an insufficient habituation to new stimuli during the first seconds of exposure. In addition, our results highlight the relevance of the orbitofrontal cortex in social anxiety disorders.     

Choline Transporter regulates olfactory habituation via a neuronal triad of excitatory,inhibitory and mushroom body neurons

Choline is an essential component of Acetylcholine (ACh) biosynthesis pathway which requires high-affinity Choline transporter (ChT) for its uptake into the presynaptic terminals of cholinergic neurons. Previously, we had reported a predominant expression of ChT in memory processing and storing region of the Drosophila brain called mushroom bodies (MBs). It is unknown how ChT contributes to the functional principles of MB operation. Here, we demonstrate the role of ChT in Habituation, a non-associative form of learning. Odour driven habituation traces are laid down in ChT dependent manner in antennal lobes (AL), projection neurons (PNs), and MBs. We observed that reduced habituation due to knock-down of ChT in MBs causes hypersensitivity towards odour, suggesting that ChT also regulates incoming stimulus suppression. Importantly, we show for the first time that ChT is not unique to cholinergic neurons but is also required in inhibitory GABAergic neurons to drive habituation behaviour. Our results support a model in which ChT regulates both habituation and incoming stimuli through multiple circuit loci via an interplay between excitatory and inhibitory neurons. Strikingly, the lack of ChT in MBs shows characteristics similar to the major reported features of Autism spectrum disorders (ASD), including attenuated habituation, sensory hypersensitivity as well as defective GABAergic signalling. Our data establish the role of ChT in habituation and suggest that its dysfunction may contribute to neuropsychiatric disorders like ASD.     

Normalization regulates competition for visual awareness

Signals in our brain are in a constant state of competition, including those that vie for motor control, sensory dominance, and awareness. To shed light on the mechanisms underlying neural competition, we exploit binocular rivalry, a phenomenon that allows us to probe the competitive process that ordinarily transpires outside of our awareness. By measuring psychometric functions under different states of rivalry, we discovered a pattern of gain changes that are consistent with a model of competition in which attention interacts with normalization processes, thereby driving the ebb and flow between states of awareness. Moreover, we reveal that attention plays a crucial role in modulating competition; without attention, rivalry suppression for high-contrast stimuli is negligible. We propose a framework whereby our visual awareness of competing sensory representations is governed by a common neural computation: normalization.     

Attention Wins over Sensory Attenuation in a Sound Detection Task

‘Sensory attenuation’, i.e., reduced neural responses to self-induced compared to externally generated stimuli, is a well-established phenomenon. However, very few studies directly compared sensory attenuation with attention effect, which leads to increased neural responses. In this study, we brought sensory attenuation and attention together in a behavioural auditory detection task, where both effects were quantitatively measured and compared. The classic auditory attention effect of facilitating detection performance was replicated. When attention and sensory attenuation were both present, attentional facilitation decreased but remained significant. The results are discussed in the light of current theories of sensory attenuation.     

Sparsity and Compressed Coding in Sensory Systems

Considering that many natural stimuli are sparse, can a sensory system evolve to take advantage of this sparsity? We explore this question and show that significant downstream reductions in the numbers of neurons transmitting stimuli observed in early sensory pathways might be a consequence of this sparsity. First, we model an early sensory pathway using an idealized neuronal network comprised of receptors and downstream sensory neurons. Then, by revealing a linear structure intrinsic to neuronal network dynamics, our work points to a potential mechanism for transmitting sparse stimuli, related to compressed-sensing (CS) type data acquisition. Through simulation, we examine the characteristics of networks that are optimal in sparsity encoding, and the impact of localized receptive fields beyond conventional CS theory. The results of this work suggest a new network framework of signal sparsity, freeing the notion from any dependence on specific component-space representations. We expect our CS network mechanism to provide guidance for studying sparse stimulus transmission along realistic sensory pathways as well as engineering network designs that utilize sparsity encoding.     

Decision, sensation, and habituation: a multi-layer dynamic field model for Inhibition of Return

Inhibition of Return (IOR) is one of the most consistent and widely studied effects in experimental psychology. The effect refers to a delayed response to visual stimuli in a cued location after initial priming at that location. This article presents a dynamic field model for IOR. The model describes the evolution of three coupled activation fields. The decision field, inspired by the intermediate layer of the superior colliculus, receives endogenous input and input from a sensory field. The sensory field, inspired by earlier sensory processing, receives exogenous input. Habituation of the sensory field is implemented by a reciprocal coupling with a third field, the habituation field. The model generates IOR because, due to the habituation of the sensory field, the decision field receives a reduced target-induced input in cue-target-compatible situations. The model is consistent with single-unit recordings of neurons of monkeys that perform IOR tasks. Such recordings have revealed that IOR phenomena parallel the activity of neurons in the intermediate layer of the superior colliculus and that neurons in this layer receive reduced input in cue-target-compatible situations. The model is also consistent with behavioral data concerning temporal expectancy effects. In a discussion, the multi-layer dynamic field account of IOR is used to illustrate the broader view that behavior consists of a tuning of the organism to the environment that continuously and concurrently takes place at different spatiotemporal scales.     

Mechanisms for allocating auditory attention: an auditory saliency map

Our nervous system is confronted with a barrage of sensory stimuli, but neural resources are limited and not all stimuli can be processed to the same extent. Mechanisms exist to bias attention toward the particularly salient events, thereby providing a weighted representation of our environment. Our understanding of these mechanisms is still limited, but theoretical models can replicate such a weighting of sensory inputs and provide a basis for understanding the underlying principles. Here, we describe such a model for the auditory system-an auditory saliency map. We experimentally validate the model on natural acoustical scenarios, demonstrating that it reproduces human judgments of auditory saliency and predicts the detectability of salient sounds embedded in noisy backgrounds. In addition, it also predicts the natural orienting behavior of naive macaque monkeys to the same salient stimuli. The structure of the suggested model is identical to that of successfully used visual saliency maps. Hence, we conclude that saliency is determined either by implementing similar mechanisms in different unisensory pathways or by the same mechanism in multisensory areas. In any case, our results demonstrate that different primate sensory systems rely on common principles for extracting relevant sensory events.     

Neuronal mechanisms of voice control are affected by implicit expectancy of externally triggered perturbations in auditory feedback

Accurate vocal production relies on several factors including sensory feedback and the ability to predict future challenges to the control processes. Repetitive patterns of perturbations in sensory feedback by themselves elicit implicit expectations in the vocal control system regarding the timing, quality and direction of perturbations. In the present study, the predictability of voice pitch-shifted auditory feedback was experimentally manipulated. A block of trials where all pitch-shift stimuli were upward, and therefore predictable was contrasted against an unpredictable block of trials in which the stimulus direction was randomized between upward and downward pitch-shifts. It was found that predictable perturbations in voice auditory feedback led to a reduction in the proportion of compensatory vocal responses, which might be indicative of a reduction in vocal control. The predictable perturbations also led to a reduction in the magnitude of the N1 component of cortical Event Related Potentials (ERP) that was associated with the reflexive compensations to the perturbations. We hypothesize that formation of expectancy in our study is accompanied by involuntary allocation of attentional resources occurring as a result of habituation or learning, that in turn trigger limited and controlled exploration-related motor variability in the vocal control system.     

More Meditation,Less Habituation? The Effect of Mindfulness Practice on the Acoustic Startle Reflex

BackgroundMindfulness as a mode of sustained and receptive attention promotes openness to each incoming stimulus, even if repetitive and/or aversive. Mindful attention has been shown to attenuate sensory habituation in expert meditators; however, others were not able to replicate this effect. The present study used acoustic startle reflex to investigate the effect of mindfulness practice intensity on sensory habituation.MethodsAuditory Startle Response (ASR) to 36 startling probes (12 trials x 3 block with 40ms inter-block intervals), was measured using electromyography (EMG) in three groups of participants (N = 12/group): meditation-naïve, moderate practice, and intensive practice.ResultsIntensive practice group showed attenuated startle habituation as evidenced by significantly less habituation over the entire experiment relative to the meditation-naïve and moderate practice groups. Furthermore, there was a significant linear effect showing between-block habituation in meditation-naïve and moderate practice groups, but not in the intensive practice group. However, the Block x Group interaction between the intensive practice and the meditation-naive groups was not significant. Moderate practice group was not significantly different from the meditation-naïve in the overall measure of habituation, but showed significantly stronger habituation than both meditation-naïve and intensive practice groups in Block 1. Greater practice intensity was significantly correlated with slower overall habituation and habituation rate in Blocks 2 and 3 in the intensive, but not in the moderate, practice group.ConclusionsThe study provides tentative evidence that intensive mindfulness practice attenuates acoustic startle habituation as measured by EMG, but the effect is modest. Moderate practice, on the other hand, appears to enhance habituation, suggesting the effect of mindfulness practice on startle habituation might be non-liner. Better understanding of the effect of mindful attention on startle habituation may shed new light on sensory information processing capacity of the human brain and its potential for de-automatisation of hard-wired processes.     

Decrease in excitability of LG following habituation of the crayfish escape reaction

Crayfish escapes from threatening stimuli to the abdomen by tailflipping upwards and forwards. This lateral giant (LG)-mediated escape reaction habituates readily upon repetitive sensory stimulation. Using an isolated abdominal nerve cord preparation, we have analyzed the change in LG activity by applying additional sensory stimulation after different periods following habituation to characterize the retention of LG habituation. Results show that the LG mediated response habituates more quickly, but the retention time is shorter, as repetitive sensory stimulation is applied at progressively shorter inter-stimulus time intervals. The spike response of LG recovers quickly, within several minutes after habituation, but they fail to spike when an additional stimulus is applied after specific long periods following habituation. The critical period of the delay for this decrease in excitability of LG is dependent on the inter-stimulus time interval of the initial repetitive stimulus. As the inter-stimulus interval became longer, the delay needed for decrease in excitability became shorter. Furthermore, the local injection of 10^–6 mol l^–1 octopamine into the neuropil just following habituation promotes the achievement of decrease in excitability. No effects were observed when 10^–6 mol l^–1 serotonin and tyramine were injected. These results suggested octopamine promotes decrease in excitability of LG following habituation.     

Habituation and prepulse inhibition of acoustic startle in rodents

The acoustic startle response is a protective response, elicited by a sudden and intense acoustic stimulus. Facial and skeletal muscles are activated within a few milliseconds, leading to a whole body flinch in rodents(1). Although startle responses are reflexive responses that can be reliably elicited, they are not stereotypic. They can be modulated by emotions such as fear (fear potentiated startle) and joy (joy attenuated startle), by non-associative learning processes such as habituation and sensitization, and by other sensory stimuli through sensory gating processes (prepulse inhibition), turning startle responses into an excellent tool for assessing emotions, learning, and sensory gating, for review see( 2, 3). The primary pathway mediating startle responses is very short and well described, qualifying startle also as an excellent model for studying the underlying mechanisms for behavioural plasticity on a cellular/molecular level(3). We here describe a method for assessing short-term habituation, long-term habituation and prepulse inhibition of acoustic startle responses in rodents. Habituation describes the decrease of the startle response magnitude upon repeated presentation of the same stimulus. Habituation within a testing session is called short-term habituation (STH) and is reversible upon a period of several minutes without stimulation. Habituation between testing sessions is called long-term habituation (LTH)(4). Habituation is stimulus specific(5). Prepulse inhibition is the attenuation of a startle response by a preceding non-startling sensory stimulus(6). The interval between prepulse and startle stimulus can vary from 6 to up to 2000 ms. The prepulse can be any modality, however, acoustic prepulses are the most commonly used. Habituation is a form of non-associative learning. It can also be viewed as a form of sensory filtering, since it reduces the organisms' response to a non-threatening stimulus. Prepulse inhibition (PPI) was originally developed in human neuropsychiatric research as an operational measure for sensory gating(7). PPI deficits may represent the interface of "psychosis and cognition" as they seem to predict cognitive impairment(8-10). Both habituation and PPI are disrupted in patients suffering from schizophrenia(11), and PPI disruptions have shown to be, at least in some cases, amenable to treatment with mostly atypical antipsychotics(12, 13). However, other mental and neurodegenerative diseases are also accompanied by disruption in habituation and/or PPI, such as autism spectrum disorders (slower habituation), obsessive compulsive disorder, Tourette's syndrome, Huntington's disease, Parkinson's disease, and Alzheimer's Disease (PPI)(11, 14, 15) Dopamine induced PPI deficits are a commonly used animal model for the screening of antipsychotic drugs(16), but PPI deficits can also be induced by many other psychomimetic drugs, environmental modifications and surgical procedures.     

The effect of disconnecting the hippocampus from the septum on the activity of septal neurons]

Extracellular recording of neuronal activity was performed in the medial and lateral septal nuclei (MS and LS) in unanaesthetized rabbits after coagulation of septo-hippocampal connections. The MS neuronal activity had many pathological features. The LS activity was normal in every respect. Spontaneous activity, reactivity to sensory stimuli and main characteristics of responses to sensory stimuli were preserved in LS (and in a part of MS neurones). Sensory effects were augmented in intensity and duration, the number of neurones in LS with theta-bursts increased twofold, theta-bursts were more regular, than in control animals. These effects may be explained by an increase of ascending RF influences, which is supported by the fact of outstanding similarity between sensory and reticular effects in septal neurones after hippocampal disconnection. The number of units with inhibition of activity in response to sensory stimuli decreased, habituation of responses was absent. That means that hippocampal influences are necessary for the organization of inhibitory phenomena in the septum, and, above all, for processes of gradual habituation.     

Development of gaze following abilities in wolves (Canis lupus)

The ability to coordinate with others' head and eye orientation to look in the same direction is considered a key step towards an understanding of others mental states like attention and intention. Here, we investigated the ontogeny and habituation patterns of gaze following into distant space and behind barriers in nine hand-raised wolves. We found that these wolves could use conspecific as well as human gaze cues even in the barrier task, which is thought to be more cognitively advanced than gazing into distant space. Moreover, while gaze following into distant space was already present at the age of 14 weeks and subjects did not habituate to repeated cues, gazing around a barrier developed considerably later and animals quickly habituated, supporting the hypothesis that different cognitive mechanisms may underlie the two gaze following modalities. More importantly, this study demonstrated that following another individuals' gaze around a barrier is not restricted to primates and corvids but is also present in canines, with remarkable between-group similarities in the ontogeny of this behaviour. This sheds new light on the evolutionary origins of and selective pressures on gaze following abilities as well as on the sensitivity of domestic dogs towards human communicative cues.     

Selective Attention Modulates the Direction of Audio-Visual Temporal Recalibration

Temporal recalibration of cross-modal synchrony has been proposed as a mechanism to compensate for timing differences between sensory modalities. However, far from the rich complexity of everyday life sensory environments, most studies to date have examined recalibration on isolated cross-modal pairings. Here, we hypothesize that selective attention might provide an effective filter to help resolve which stimuli are selected when multiple events compete for recalibration. We addressed this question by testing audio-visual recalibration following an adaptation phase where two opposing audio-visual asynchronies were present. The direction of voluntary visual attention, and therefore to one of the two possible asynchronies (flash leading or flash lagging), was manipulated using colour as a selection criterion. We found a shift in the point of subjective audio-visual simultaneity as a function of whether the observer had focused attention to audio-then-flash or to flash-then-audio groupings during the adaptation phase. A baseline adaptation condition revealed that this effect of endogenous attention was only effective toward the lagging flash. This hints at the role of exogenous capture and/or additional endogenous effects producing an asymmetry toward the leading flash. We conclude that selective attention helps promote selected audio-visual pairings to be combined and subsequently adjusted in time but, stimulus organization exerts a strong impact on recalibration. We tentatively hypothesize that the resolution of recalibration in complex scenarios involves the orchestration of top-down selection mechanisms and stimulus-driven processes.