Voluntary control of attention promotes intelligent, adaptive behaviors by enabling the selective processing of information that is most relevant for making decisions. Despite extensive research on attention in primates, the capacity for selective attention in nonprimate species has never been quantified. Here we demonstrate selective attention in chickens by applying protocols that have been used to characterize visual spatial attention in primates. Chickens were trained to localize and report the vertical position of a target in the presence of task-relevant distracters. A spatial cue, the location of which varied across individual trials, indicated the horizontal, but not vertical, position of the upcoming target. Spatial cueing improved localization performance: accuracy (d′) increased and reaction times decreased in a space-specific manner. Distracters severely impaired perceptual performance, and this impairment was greatly reduced by spatial cueing. Signal detection analysis with an "indecision" model demonstrated that spatial cueing significantly increased choice certainty in localizing targets. By contrast, error-aversion certainty (certainty of not making an error) remained essentially constant across cueing protocols, target contrasts, and individuals. The results show that chickens shift spatial attention rapidly and dynamically, following principles of stimulus selection that closely parallel those documented in primates. The findings suggest that the mechanisms that control attention have been conserved through evolution, and establish chickens-a highly visual species that is easily trained and amenable to cutting-edge experimental technologiesas an attractive model for linking behavior to neural mechanisms of selective attention.T he capacity to select particular locations or stimuli for differential analysis and decision making is essential for any animal to behave intelligently in a complex environment. It follows that neural mechanisms that enable this capacity must have appeared early in evolution (1). In humans, and nonhuman primates, selective attention enables such adaptive behavior by selecting from all possible information the information that is most relevant for making decisions (2, 3). However, little is known about whether the capacity for selective attention exists in nonprimate vertebrate species.Studies that were intended to measure selective attention in nonprimate species have produced inconclusive results for several reasons. First, much of the previous work has inferred the capacity for selective attention based on selective learning or selective reporting of specific cue features, both in birds (4) and in rodents (5). For example, in highly cited work on feature-based attention (4), pigeons were reinforced for pecking on targets that contained combinations of two features (e.g., color and shape). In later trials, when the features were presented individually, they pecked almost exclusively on targets with only one of the two features (e.g., color, ignoring shape). The results ...
Sensory systems do not develop and function independently of one another, yet they are typically studied in isolation. Effects of multisensory interactions on the developing neocortex can be revealed by altering the ratios of incoming sensory inputs associated with different modalities. We investigated neural responses in primary somatosensory cortex (S1) of short-tailed opossums (; either sex) after the elimination of visual input through bilateral enucleation very early in development. To assess the influence of tactile experience after vision loss, we also examined naturally occurring patterns of exploratory behavior. In early blind (EB) animals, overall levels of tactile experience were similar to those of sighted controls (SC); locomotor activity was unimpaired and accompanied by whisking. Using extracellular single-unit recording techniques under anesthesia, we found that EB animals exhibited a reduction in the magnitude of neural responses to whisker stimuli in S1, coupled with spatial sharpening of receptive fields, in comparison to SC animals. These alterations manifested as two different effects on sensory processing in S1 of EB animals: the ability of neurons to detect single whisker stimulation was decreased, whereas their ability to discriminate between stimulation of neighboring whiskers was enhanced. The increased selectivity of S1 neurons in EB animals was reflected in improved population decoding performance for whisker stimulus position, particularly along the rostrocaudal axis of the snout, which aligns with the primary axis of natural whisker motion. These findings suggest that a functionally distinct form of somatosensory plasticity occurs when vision is lost early in development. After sensory loss, compensatory behavior mediated through the spared senses could be generated entirely through the recruitment of brain areas associated with the deprived sense. Alternatively, functional compensation in spared modalities may be achieved through a combination of plasticity in brain areas corresponding to both spared and deprived sensory modalities. Although activation of neurons in cortex associated with a deprived sense has been described frequently, it is unclear whether this is the only substrate available for compensation or if plasticity within cortical fields corresponding to spared modalities, particularly primary sensory cortices, may also contribute. Here, we demonstrate empirically that early loss of vision alters coding of sensory inputs in primary somatosensory cortex in a manner that supports enhanced tactile discrimination.
The mammalian auditory cortex is necessary for spectral and spatial processing of acoustic stimuli. Most physiological studies of single neurons in the auditory cortex have focused on the onset and sustained portions of evoked responses, but there have been far fewer studies on the relationship between onset and offset responses. In the current study, we compared spectral and spatial tuning of onset and offset responses of neurons in primary auditory cortex (A1) and the caudolateral (CL) belt area of awake macaque monkeys. Several different metrics were used to determine the relationship between onset and offset response profiles in both frequency and space domains. In the frequency domain, a substantial proportion of neurons in A1 and CL displayed highly dissimilar best stimuli for onset- and offset-evoked responses, although even for these neurons, there was usually a large overlap in the range of frequencies that elicited onset, and offset responses and distributions of tuning overlap metrics were mostly unimodal. In the spatial domain, the vast majority of neurons displayed very similar best locations for onset- and offset-evoked responses, along with unimodal distributions of all tuning overlap metrics considered. Finally, for both spectral and spatial tuning, a slightly larger fraction of neurons in A1 displayed nonoverlapping onset and offset response profiles, relative to CL, which supports hierarchical differences in the processing of sounds in the two areas. However, these differences are small compared with differences in proportions of simple cells (low overlap) and complex cells (high overlap) in primary and secondary visual areas. In the current study, we examine the relationship between the tuning of neural responses evoked by the onset and offset of acoustic stimuli in the primary auditory cortex, as well as a higher-order auditory area-the caudolateral belt field-in awake rhesus macaques. In these areas, the relationship between onset and offset response profiles in frequency and space domains formed a continuum, ranging from highly overlapping to highly nonoverlapping.
Movable tactile sensors in the form of whiskers are present in most mammals, but sensory coding in the cortical whisker representation has been studied almost exclusively in mice and rats. Many species that possess whiskers lack the modular “barrel” organization found in the primary somatosensory cortex (S1) of mice and rats, but it is unclear how whisker-related input is represented in these species. We used single-unit extracellular recording techniques to characterize receptive fields and response properties in S1 of Monodelphis domestica (short-tailed opossum), a nocturnal, terrestrial marsupial that shared its last common ancestor with placental mammals over 160 million years ago. Short-tailed opossums lack barrels and septa in S1, but show active whisking behavior similar to mice and rats. Most neurons in short-tailed opossum S1 exhibited multiwhisker receptive fields, including a single best whisker and lower magnitude responses to the deflection of surrounding whiskers. Mean tuning width was similar to that reported in mice and rats. Both symmetrical and asymmetrical receptive fields were present. Neurons tuned to ventral whiskers tended to show broad tuning along the rostrocaudal axis. Thus, despite the absence of barrels, most receptive field properties were similar to those reported in mice and rats. However, unlike those species, S1 neuronal responses to best whisker and surround whisker deflection showed comparable latencies in short-tailed opossums. This dissimilarity suggests that some aspects of barrel cortex function may not generalize to tactile processing across mammalian species, and may be related to differences in the architecture of the whisker-to-cortex pathway.
Purpose To perform in vivo evaluation of the structural morphology and vascular plexuses of the neurosensory retina and choroid across vertebrate species using swept-source optical coherence tomography (SS-OCT) and SS-OCT angiography (SS-OCTA) imaging. Methods A custom-built SS-OCT system with an incorporated flexible imaging arm was used to acquire the three-dimensional (3D) retinal OCT and vascular OCTA data of five different vertebrates: a mouse (C57BL/6J), a rat (Long Evans), a gray short-tailed opossum ( Monodelphis domestica ), a white sturgeon ( Acipenser transmontanus ), and a great horned owl ( Bubo virginianus ). Results In vivo structural morphology of the retina and choroid, as well as en face OCTA images of retinal and choroidal vasculature of all species were generated. The retinal morphology and vascular plexuses were similar between rat and mouse, whereas distinct choroidal and paired superficial vessels were observed in the opossum retina. The retinal and vascular structure of the sturgeon, as well as the pecten oculi and overlying the avascular and choroidal vasculature in the owl retina are reported in vivo. Conclusions A high-quality two-dimensional and 3D in vivo visualization of the retinal structures and en face visualization of the retina and choroidal vascular plexus of vertebrates was possible. Our studies affirm that SS-OCT and SS-OCTA are viable methods for evaluating the in vivo retinal and choroidal structure across terrestrial, aquatic, and aerial vertebrates. Translational Relevance In vivo characterization of retinal morphology and vasculature plexus of multiple species using SS-OCT and SS-OCTA imaging can increase the pool of species available as models of human retinal diseases.
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