Sequential maturation of stimulus-specific adaptation in the mouse lemniscal auditory system.

Stimulus-specific adaptation (SSA), the reduction of neural activity to a common stimulus that does not generalize to other, rare stimuli, is an essential property of our brain. Although well characterized in adults, it is still unknown how it develops during adolescence and what neuronal circuits are involved. Using in vivo electrophysiology and optogenetics in the lemniscal pathway of the mouse auditory system, we observed SSA to be stable from postnatal day 20 (P20) in the inferior colliculus, to develop until P30 in the auditory thalamus and even later in the primary auditory cortex (A1). We found this maturation process to be experience-dependent in A1 but not in thalamus and to be related to alterations in deep but not input layers of A1. We also identified corticothalamic projections to be implicated in thalamic SSA development. Together, our results reveal different circuits underlying the sequential SSA maturation and provide a unique perspective to understand predictive coding and surprise across sensory systems.

Task-induced modulations of neuronal activity along the auditory pathway.

Sensory processing varies depending on behavioral context. Here, we ask how task engagement modulates neurons in the auditory system. We train mice in a simple tone-detection task and compare their neuronal activity during passive hearing and active listening. Electrophysiological extracellular recordings in the inferior colliculus, medial geniculate body, primary auditory cortex, and anterior auditory field reveal widespread modulations across all regions and cortical layers and in both putative regular- and fast-spiking cortical neurons. Clustering analysis unveils ten distinct modulation patterns that can either enhance or suppress neuronal activity. Task engagement changes the tone-onset response in most neurons. Such modulations first emerge in subcortical areas, ruling out cortical feedback as the only mechanism underlying subcortical modulations. Half the neurons additionally display late modulations associated with licking, arousal, or reward. Our results reveal the presence of functionally distinct subclasses of neurons, differentially sensitive to specific task-related variables but anatomically distributed along the auditory pathway.

Dynamic Contextual Modulation in Superior Colliculus of Awake Mouse.

The responses of neurons in the visual pathway depend on the context in which a stimulus is presented. Responses to predictable stimuli are usually suppressed, highlighting responses to unexpected stimuli that might be important for behavior. Here, we established how context modulates the response of neurons in the superior colliculus (SC), a region important in orienting toward or away from visual stimuli. We made extracellular recordings from single units in the superficial layers of SC in awake mice. We found strong suppression of visual response by spatial context (surround suppression) and temporal context (adaptation). Neurons showing stronger surround suppression also showed stronger adaptation effects. In neurons where it was present, surround suppression was dynamic and was reduced by adaptation. Adaptation's effects further revealed two components to surround suppression: one component that was weakly tuned for orientation and adaptable, and another component that was more strongly tuned but less adaptable. The selectivity of the tuned component was flexible, such that suppression was stronger when the stimulus over the surround matched that over the receptive field. Our results therefore reveal strong interactions between spatial and temporal context in regulating the flow of signals through mouse SC, and suggest the presence of a subpopulation of neurons that might signal novelty in either space or time.

Visual response properties of neurons in the superficial layers of the superior colliculus of awake mouse.

KEY POINTS: In rodents, including mice, the superior colliculus is the major target of the retina, but its visual response is not well characterized. In the present study, extracellular recordings from single nerve cells in the superficial layers of the superior colliculus were made in awake, head-restrained mice, and their responses to visual stimuli were measured. It was found that these neurons show brisk, highly sensitive and short latency visual responses, a preference for black over white stimuli, and diverse responses to moving patterns. At least five broad classes can be defined by variation in functional properties among units. The results of the present study demonstrate that eye movements have a measurable impact on visual responses in awake animals and show how they may be mitigated in analyses. ABSTRACT: The mouse is an increasingly important animal model of visual function in health and disease. In mice, most retinal signals are routed through the superficial layers of the midbrain superior colliculus, and it is well established that much of the visual behaviour of mice relies on activity in the superior colliculus. The functional organization of visual signals in the mouse superior colliculus is, however, not well established in awake animals. We therefore made extracellular recordings from the superficial layers of the superior colliculus in awake mice, while the animals were viewing visual stimuli including flashed spots and drifting gratings. We find that neurons in the superficial layers of the superior colliculus of awake mouse generally show short latency, brisk responses. Receptive fields are usually 'ON-OFF' with a preference for black stimuli, and are weakly non-linear in response to gratings and other forms of luminance modulation. Population responses to drifting gratings are highly contrast sensitive, with a robust response to spatial frequencies above 0.3 cycles degree-1 and temporal frequencies above 15 Hz. The receptive fields are also often speed-tuned or direction-selective. Analysis of the response across multiple stimulus dimensions reveals at least five functionally distinct groups of units. We also find that eye movements affect measurements of receptive field properties in awake animals, and show how these may be mitigated in analyses. Qualitatively similar responses were obtained in urethane-anaesthetized animals, although receptive fields in awake animals had higher contrast sensitivity, shorter visual latency and a stronger response to high temporal frequencies.

Emergence of transformation-tolerant representations of visual objects in rat lateral extrastriate cortex.

Rodents are emerging as increasingly popular models of visual functions. Yet, evidence that rodent visual cortex is capable of advanced visual processing, such as object recognition, is limited. Here we investigate how neurons located along the progression of extrastriate areas that, in the rat brain, run laterally to primary visual cortex, encode object information. We found a progressive functional specialization of neural responses along these areas, with: (1) a sharp reduction of the amount of low-level, energy-related visual information encoded by neuronal firing; and (2) a substantial increase in the ability of both single neurons and neuronal populations to support discrimination of visual objects under identity-preserving transformations (e.g., position and size changes). These findings strongly argue for the existence of a rat object-processing pathway, and point to the rodents as promising models to dissect the neuronal circuitry underlying transformation-tolerant recognition of visual objects.

Vision Guides Selection of Freeze or Flight Defense Strategies in Mice.

In prey species such as mice, avoidance of predators is key to survival and drives instinctual behaviors like freeze or flight [1, 2]. Sensory signals guide the selection of appropriate behavior [3], and for aerial predators only vision provides useful information. Surprisingly, there is no evidence that vision can guide the selection of escape strategies. Fleeing behavior can be readily triggered by a rapidly looming overhead stimulus [4]. Freezing behavior, however, has previously been induced by real predators or their odors [5]. Here, we discover that a small moving disk, simulating the sweep of a predator cruising overhead, is sufficient to induce freezing response in mice. Looming and sweeping therefore provide visual triggers for opposing flight and freeze behaviors and provide evidence that mice innately make behavioral choices based on vision alone. VIDEO ABSTRACT.