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Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties
Abstract
Neuroanatomical studies have demonstrated that the two major descending pathways from the superior colliculus arise from regionally segregated, distinct, cells of origin. Stimulation and lesion studies have implicated the crossed descending tecto-reticulo-spinal projection in approach movements towards novel stimuli whereas the ipsilateral pathway appears to be involved in the control of avoidance and escape-like behaviours. The present electrophysiological study attempted to characterise the sensory properties of antidromically identified cells of origin of these pathways in anaesthetised rats. We found that the contralaterally projecting predorsal bundle (PDB) efferents were primarily somatosensory while the ipsilateral cuneiform (CNF) projection was primarily visual. PDB cells, mainly found in the intermediate layers, responded principally to vibrissal stimulation with their overlying visual fields optimally stimulated by small dark moving objects in the lower rostral and lateral field. In contrast, most CNF cells were located rostromedially, with the greatest contribution from visual cells responsive to stimuli in the upper rostral field. A significant proportion of these showed no response to small moving dark discs but fired vigorously to 'looming' stimuli. Ethological considerations suggest that these are appropriate stimulus characteristics for a system controlling approach and avoidance behaviour in an animal such as the rat where predators generally appear from above and prey is found on the ground.
... A seminal study identified four different cell types in the superficial SC based on morphology, receptive field properties and projection patterns (Gale and Murphy, 2014). Another group described neurons specifically tuned to respond to dark expanding looming spots (Westby et al., 1990;Zhao et al., 2014). Many of these visual properties of SC neurons are derived from their RGC inputs, but some few might also be generated locally (Gale and Murphy, 2016). ...
... In mammals, the superior colliculus has been identified as the main brain area responsible for detecting the visual looming stimulus (Figure 1.3, Westby et al., 1990;Zhao et al., 2014;Pereira and Moita, 2016;Branco and Redgrave, 46 2020). The SC is a highly conserved midbrain structure organised in topographically arranged functional layers (May, 2006;Ito and Feldheim, 2018). ...
... Looming-sensitivity is inherited by some SC neurons, which show strong selectivity to the stimulus in several vertebrate species (Westby et al., 1990;Kang and Li, 2010;Liu et al., 2011;Zahar et al., 2012;Zhao et al., 2014;Temizer et al., 2015;Dunn et al., 2016;Evans et al., 2018;Suzuki et al., 2019). ...
Animals can react differently to similar sensory information depending on behavioural circumstances and previous experience. This flexibility is thought to depend on neural inhibition, through suppression of inappropriate and disinhibition of appropriate actions. In this thesis, I identified the ventral lateral geniculate nucleus (vLGN), an inhibitory prethalamic area, as a critical node for the control of visually evoked defensive responses in mice. First, I characterised the structural and functional organisation of the vLGN. Then, taking advantage of a well-characterised model for instinctive behavioural decisions – escape from imminent threat – I showed that GABAergic projections from vLGN to the medial superior colliculus (mSC), a known hub for threat-evoked defensive behaviours, convey information about previous experience of threat and assessment of risk in the environment. Activity in these projections was reduced when mice had experienced a threatening stimulus, while it was elevated after mice learned that stimuli did not pose any danger. Consistently, the chemogenetic suppression of vLGN activity increased risk-avoidance behaviour. The optogenetic activation of vLGN abolished escape responses to imminent visual threats, while suppressing vLGN activity increased the escape probability, demonstrating that vLGN exerts strong, bidirectional control over escape responses. Moreover, electrophysiological mSC recordings in vivo during optogenetic stimulation of vLGN, revealed that vLGN specifically suppresses the activity of visually responsive but not auditory-responsive neurons in the mSC. The optogenetic manipulation of GABAergic projections from vLGN to mSC more strongly influenced escape responses to visual than to auditory threats, suggesting a specificity of this pathway for visually guided behaviours. Together, these results indicate that vLGN flexibly controls the threshold for instinctive responses to imminent visual threat, depending on the animal’s prior experience and its anticipation of danger in the environment. These findings significantly strengthen the circuit-level understanding of flexible behaviour, and how different types of information are integrated to inform decisions.
... Accordingly, the superior colliculus and its analogue in other species (the optic tectum) seem to be the primary brain region responsible for detecting threatening looming stimuli (Westby et al., 1990;Wu et al., 2005). The superficial layers of the superior colliculus receive direct input from the OFF-channel retinal ganglion cells, which are highly sensitive to looming visual stimuli (Yilmaz and Meister, 2013). ...
... In turn, the neurons of the superior colliculus inherit this sensitivity to looming stimuli Westby et al., 1990;Zhao, Liu, and Cang, 2014). The neurons in the deep superior colliculus project to brainstem structures involved with premotor activity and the initiation of movements, such as the periaquectal gray, providing a rapid route from detection of a threat to action. ...
Executing appropriate defensive actions is vital for survival. In mice, imminent threat elicits fast and accurate escape behaviour that relies on a rapidly formed spatial memory to reach shelter locations. I investigated the navigational strategies used by mice to navigate to safety upon imminent threat, and the role of the hippocampal formation – classically associated with spatial representations – in guiding escape navigation. Through a series of behavioural experiments designed to distinguish between navigational strategies guiding escape, I found that while flight was consistent during the the first 800ms across light and dark conditions, visual cues enabled faster, more efficient escape trajectories later on in flight, suggesting escape has two phases: orienting and accelerating towards the shelter, relying on a memorised vector; and a second phase using vision to refine escape trajectories. Accordingly, I found that path integration was necessary for navigation in the dark, but not in the light. I next investigated the dependency of escape on brain structures associated with spatial representation in the hippocampal formation. An abrupt lesion targeted to the hippocampus using ibotenic acid disrupted escape navigation. A more targeted lesion of the primary hippocampal output - an infusion of muscimol into the subiculum – also led to a disruption of escape navigation and an increased propensity to freeze in response to looming visual stimuli. Finally, while disrupting neural activity in the subiculum by stimulating with channelrhodopsin reduced acceleration, this effect was present with optogenetic stimulation alone, precluding any firm conclusions from these experiments with respect to escape navigation. Together, these data further our knowledge of defensive behaviours in mice by implicating high-level spatial representations of the environment in guiding escape navigation, identifying behavioural signatures of navigational strategies requiring these representations, and showing the dependency of escape navigation on brain regions associated with spatial representations.
... Indeed, most animals, including mammals, reptiles, fish, fruit flies, locusts, and barnacles, respond defensively to looming stimuli, demonstrating their evolutionary warning roles in threat processing. Chickens flap their wings in fright, monkeys raise their arms, cockroaches flee potential predators, and barnacles close their shells (e.g., Ball & Tronick, 1971;Card & Dickenson, 2008;Dill, 1990;Gwilliam, 1963;Westby et al., 1990). Even human infants as young as 4-6 months of age, exhibit avoidance responses to looming sounds but not to other equivalent sounds (Freiberg et al., 2001;Joen et al., 2000;Schmuckler et al., 2007), and young children display greater stranger anxiety to unfamiliar persons who approach them rapidly rather than slowly (Reingold & Eckerman, 1973;Trause, 1977). ...
Background
A revised looming vulnerability model is described that updates the original conceptual model and synthesizes new findings and evidence. The revised model extends the notion of dynamic threat by describing the role of cognitive-perceptual distortions. Moreover, it suggests that dynamic threat perceptions, particularly that threats are approaching, serve as warning signals that lower the threshold for appraising threat, influencing negative emotional responses (primarily but not only anxiety and fear), cognitive-affective processing, behavior, and maladaptive coping. Individual differences in “looming cognitive style” can lead to transdiagnostic vulnerability to anxiety (and less so, to depression), maladaptive defensive reactions, cognitive-affective (experiential) avoidance, and stress generation.
Methods
This article reviews the conceptualization proposed by the revised looming vulnerability model, and comprehensively reviews its scientific foundation, and current supporting evidence that has accrued for the model across diverse research domains.
Results
The revised conceptualization of the looming vulnerability model is amply supported by the accumulated research, which highlights the importance of dynamic stimuli for attention, memory, emotional, and neurological response. Likewise, the looming cognitive style is supported by a substantial number of studies, linking it to cognitive vulnerability to anxiety, biased threat processing, maladaptive coping and cognitive-affective avoidance, and developmental antecedents.
Conclusions
The review of evidence supports the revised looming vulnerability model's tenets about the importance of dynamic stimulusi features, which previous models have neglected, and of the looming cognitive style, which is proposed as a distinct cognitive vulnerability Clinical implications and future research directions are discussed.
... Both in rodents (Sahibzada et al., 1986) and even in macaques (DesJardin et al., 2013), stimulation of the superior colliculus can induce defensive-like behaviours. In rodents, the superior colliculus has looming-sensitive neurons (Westby et al., 1990) and coordinates this defensive behaviour by transferring threat signal to the parabigeminal nucleus or the lateral posterior thalamic nucleus to activate a fleeing or freezing response (Shang et al., 2018). In marmosets, neurons of the superior colliculus show direction selectivity and have been suggested to play a role in the processing of looming stimuli (Tailby et al., 2012). ...
... More precisely, the SC is involved in integrating environmental stimuli in order to coordinate neck and eye muscle movements [22][23][24]. In addition, the decision to focus the study on the SC was due to the fact that there is considerable evidence of a connection between the respiratory centers and this structure, as it is able to initiate appropriate respiratory defensive responses in case of threatening stimuli [25,26] and to play a role in avoidance reactions [27][28][29]. Specifically, we investigated the possible presence of developmental alterations of the SC in a large set of SIDS cases compared to controls. Encouraging preliminary results were obtained, leading us to hypothesize that SC alterations can contribute to the pathogenetic mechanism of SIDS. ...
The aim of this study was to investigate the involvement of the mesencephalic superior colliculus (SC) in the pathogenetic mechanism of SIDS, a syndrome frequently ascribed to arousal failure from sleep. We analyzed the brains of 44 infants who died suddenly within the first 7 months of life, among which were 26 infants with SIDS and 18 controls. In-depth neuropathological investigations of serial sections of the midbrain showed the SC layered cytoarchitectural organization already well known in animals, as made up of seven distinct layers, but so far never highlighted in humans, albeit with some differences. In 69% of SIDS cases but never in the controls, we observed alterations of the laminar arrangement of the SC deep layers (precisely, an increased number of polygonal cells invading the superficial layers and an increased presence of intensely stained myelinated fibers). Since it has been demonstrated in experimental studies that the deep layers of the SC exert motor control including that of the head, their developmental disorder could lead to the failure of newborns who are in a prone position to resume regular breathing by moving their heads in the sleep-arousal phase. The SC anomalies highlighted here represent a new step in understanding the pathogenetic process that leads to SIDS.
... SC neurons send projections to many motor-related regions, and this may be a neuronal substrate by which the SC integrates the different motor actions of predatory hunting [66,80]. First, the contralaterally crossed descending tectofugal pathways may mediate the head movement during orienting, which is a major part of hunting initiation [81]. ...
Predatory hunting is an important type of innate behavior evolutionarily conserved across the animal kingdom. It is typically composed of a set of sequential actions, including prey search, pursuit, attack, and consumption. This behavior is subject to control by the nervous system. Early studies used toads as a model to probe the neuroethology of hunting, which led to the proposal of a sensory-triggered release mechanism for hunting actions. More recent studies have used genetically-trackable zebrafish and rodents and have made breakthrough discoveries in the neuroethology and neurocircuits underlying this behavior. Here, we review the sophisticated neurocircuitry involved in hunting and summarize the detailed mechanism for the circuitry to encode various aspects of hunting neuroethology, including sensory processing, sensorimotor transformation, motivation, and sequential encoding of hunting actions. We also discuss the overlapping brain circuits for hunting and feeding and point out the limitations of current studies. We propose that hunting is an ideal behavioral paradigm in which to study the neuroethology of motivated behaviors, which may shed new light on epidemic disorders, including binge-eating, obesity, and obsessive-compulsive disorders.
... Thus, the SC may orchestrate different motor actions for predatory hunting with divergent tectofugal pathways projecting to the downstream motor-related target regions (Dean et al., 1989;Westby et al., 1990). First, the contralaterally crossed descending tectofugal pathways to the hindbrain may be involved in the orienting movement of the head that are vital components of hunting initiation (Isa and Sasaki, 2002). ...
All animals possess a plethora of innate behaviors that do not require extensive learning and are fundamental for their survival and propagation. With the advent of newly-developed techniques such as viral tracing and optogenetic and chemogenetic tools, recent studies are gradually unraveling neural circuits underlying different innate behaviors. Here, we summarize current development in our understanding of the neural circuits controlling predation, feeding, male-typical mating, and urination, highlighting the role of genetically defined neurons and their connections in sensory triggering, sensory to motor/motivation transformation, motor/motivation encoding during these different behaviors. Along the way, we discuss possible mechanisms underlying binge-eating disorder and the pro-social effects of the neuropeptide oxytocin, elucidating the clinical relevance of studying neural circuits underlying essential innate functions. Finally, we discuss some exciting brain structures recurrently appearing in the regulation of different behaviors, which suggests both divergence and convergence in the neural encoding of specific innate behaviors. Going forward, we emphasize the importance of multi-angle and cross-species dissections in delineating neural circuits that control innate behaviors.
... One such evolutionary subcortical structure is the SC (Gharaei et al., 2018) which is responsive to stimuli from multiple sensory modalities (Rowland, Quessy, Stanford, & Stein, 2007;Wallace, Meredith et al., 1993, 1998. Research in a range of species, including humans, has shown that the SC produces not only orienting responses but defensive reactions to looming (threatening) stimuli as well (e.g., Billington, Wilkie, Field, & Wann, 2011;Comoli et al., 2012;Dean, Redgrave, Sahibzada, & Tsuji, 1986, Dean, Redgrave, Westby, 1989Liu, Wang, & Li, 2011;Westby, Keay, Redgrave, Dean, & Bannister, 1990). The defensive-reactivity of the SC might have evolved during the course of primate evolution through modification and redeployment of neural circuits or networks (Anderson, 2010;Anderson & Finlay, 2014). ...
Objective:
Neuroplasticity enables the brain to establish new crossmodal connections or reorganize old connections which are essential to perceiving a multisensorial world. The intent of this review is to identify and summarize the current developments in neuroplasticity and crossmodal connectivity, and deepen understanding of how crossmodal connectivity develops in the normal, healthy brain, highlighting novel perspectives about the principles that guide this connectivity.
Methods:
To the above end, a narrative review is carried out. The data documented in prior relevant studies in neuroscience, psychology and other related fields available in a wide range of prominent electronic databases are critically assessed, synthesized, interpreted with qualitative rather than quantitative elements, and linked together to form new propositions and hypotheses about neuroplasticity and crossmodal connectivity.
Results:
Three major themes are identified. First, it appears that neuroplasticity operates by following eight fundamental principles and crossmodal integration operates by following three principles. Second, two different forms of crossmodal connectivity, namely direct crossmodal connectivity and indirect crossmodal connectivity, are suggested to operate in both unisensory and multisensory perception. Third, three principles possibly guide the development of crossmodal connectivity into adulthood. These are labeled as the principle of innate crossmodality, the principle of evolution-driven 'neuromodular' reorganization and the principle of multimodal experience. These principles are combined to develop a three-factor interaction model of crossmodal connectivity.
Conclusions:
The hypothesized principles and the proposed model together advance understanding of neuroplasticity, the nature of crossmodal connectivity, and how such connectivity develops in the normal, healthy brain.
Background
In cognitive models, faulty threat appraisals that are associated with threat cognitions in anxiety are frequently seen as the outcome of logical errors. The looming vulnerability model expands upon such views by emphasizing the role of perceptual and phenomenological distortions in threat estimation. It assumes that anxiety is associated with cognitive-perceptual distortions of time, space, and movement (e.g., space and time compression) that heighten the subjective impression that threats are rapidly approaching, even when they aren’t. The present study was undertaken to develop an easy-to-administer and implement self-report measure to assess such perceptual distortions.Methods
University students (N = 751; 71% female) completed a battery of online questionnaires that included the Looming Vulnerability Distortions Questionnaire (LVDQ) and measures of the looming cognitive style (LCS), cognitive distortions, social desirability, anxiety, worry, intolerance of uncertainty, and depression.ResultsA bifactor ESEM model displayed excellent fit indices and reliability for the LVDQ. Although the results provided strongest support for the use of a general score over specific subscales, they also support the secondary use of some specific scores for some types of distortions. The LVDQ uniquely predicted variance in LCS, anxiety, worry, intolerance of uncertainty, and depression. Moreover, both the LVDQ and LCS also uniquely predicted scores on a face-valid lab-based task, not explained by logical reasoning distortions.Conclusions
These results support the idea that the LVDQ is a valid measure of cognitive-perceptual distortions associated with anxiety and indicate that it predicts unique variance in anxiety and other emotional distress not explained by a typical measure of logical errors. Clinical implications and future directions are discussed.
Flexibly selecting appropriate actions in response to complex, ever-changing environments requires both cortical and subcortical regions, which are typically described as participating in a strict hierarchy. In this traditional view, highly specialized subcortical circuits allow for efficient responses to salient stimuli, at the cost of adaptability and context-specificity, which are attributed to the neocortex. Their interactions are often described as the cortex providing top-down command signals for subcortical structures to implement; however, as available technologies develop, studies increasingly demonstrate that behavior is represented by brain-wide activity and that even subcortical structures contain early signals of choice, suggesting that behavioral functions emerge as a result of different regions interacting as truly collaborative networks. In this review, we discuss the field's evolving understanding of how cortical and subcortical regions in placental mammals interact cooperatively- not only via top-down cortical-subcortical inputs, but through bottom-up interactions, especially via the thalamus. We describe our current understanding of the circuitry of both the cortex and two exemplar subcortical structures- the superior colliculus and striatum- to identify which information is prioritized by which regions. We then describe the functional circuits these regions form with one another- and the thalamus- to create parallel loops and complex networks for brain-wide information flow. Finally, we challenge the classic view that functional modules are contained within specific brain regions; instead, we propose that certain regions prioritize specific types of information over others, but the subnetworks they form- defined by their anatomical connections and functional dynamics- are the basis of true specialization.
Classical ethology provides two fundamental themes which remain at the heart of current research in neuroethology. First, is the assumption that events in the sensory “Umwelt” activate behavior via narrowly-tuned stimulus filters — i.e., that relatively few distinctive features determine the recognition of food, mate, parent or enemy. The term “innate releasing mechanisms” is probably too narrow to characterize the complexity of sensory recognition schema for birds and mammals, but it still seems to apply to many behaviors of fishes, amphibians and reptiles. As an example, the feeding behavior in newly metamorphosed froglets (Ingle, unpubl. data) seems to emerge fullblown: with no prior experience as tadpoles in pursuing visual objects, they accurately turn and snap at small moving prey. These movement sequences also fit the original notion of a “fixed action pattern”, which is the second main inheritance from classical ethology. During prey-catching the frog’s coordination of head, mouth, tongue and leg movements is highly stereotyped. The patterns predictable from knowing the radial location, height and distance of the prey. Although the behavior appears rigid, it is fast and accurate: well-adapted for the rigorous competition for food and survival among a large population with limited resources.
One of the primary aims of this chapter is to bring the superior colliculus and pretectum into the main stream of conceptualization about, and experimental approach to, visual mechanisms. Recent surveys have concentrated their attention on the retinal geniculocortical part of the central visual mechanisms to the exclusion or neglect of the midbrain. For example, mention of the superior colliculus in the last edition of a classical textbook of physiology [124] is limited to two lines, and only 6 pages were addressed to this structure in an international symposium on vision in 1961 [85]. This bias is due in part to the fact that new experimental data on the colliculus have only recently become available, and in part to the classical allocation of the pretectum-superior colliculus as a visuomotor center mediating pupillary responses, eye movements and visual grasp reflexes, but uninvolved in “higher level” processing and perception. Therefore an attempt to review and synthesize the role of these structures in vision on the basis of their anatomy and physiology alone has certain difficulties which are obvious. For such a chapter to be most meaningful, it is desirable to take an overview of the entire system and to place the colliculus in proper perspective, not to isolate it. Such a comprehensive approach, however, lies beyond the space limitations of this chapter, and the reader must in large part integrate for himself these data with those contained in other chapters of this volume.
The topographical relations of the visual field with the superior colliculus of the rat was investigated using constant small visual stimuli and recording the electrical response of aggregate unit activity with fine tip metal microelectrodes. A precise essentially linear projection onto the contralateral colliculus was demonstrated after appropriate corrections for brain curvature were performed. The general pattern and arrangement of the retinotopic projection is similar to that found in infra-mammalian vertebrates. An ipsilateral projection appears to be absent. The phasic properties and rhythmic discharge patterns of single units in the coliculus were studied with stationary and moving luminous stimuli.
Lesions of the superior colliculus in rats attenuate the oral stereotypy produced by systemic administration of dopamine agonists. Current evidence suggests that such drugs affect the superior colliculus by reducing transmission in the inhibitory GABAergic nigrotectal pathway. To investigate whether the superior colliculus plays a direct role in producing stereotyped oral movements, the present experiment therefore examined the effects of collicular microinjections of the GABA antagonist picrotoxin on the behaviour of rats observed in an open-field.
Gnawing was observed after injections of picrotoxin (25 ng) into sites in the intermediate and deep layers of the superior colliculus, consistent with the superior colliculus playing a direct part in producing the stereotyped gnawing seen after systemic administration of dopamine agonists. However, gnawing was only observed after a period in which the animal showed strong avoidance reactions, to stimuli that normally evoked orienting or little reaction. This change in reactivity was observed after injections of picrotoxin into all parts of the colliculus, but the most sensitive (responding to doses as low as 12.5 ng) were mainly in the superficial and intermediate layers. It appears that there may be more than one GABAergic system within the superior colliculus.
Infants show an adaptive avoidance response to approaching objects. The response is affected by the closeness and speed of
approach. It is mediated by visual variables. Air-pressure changes do not elicit the response. This kind of response implies
discrimination and response to distal variables rather than merely to their proximal mediators.