Repetitive auditory stimulation at a critical prenatal period modulates the postnatal functional development of the auditory as well as visual system in chicks (Gallus domesticus)

The extrinsic sensory stimulation plays a crucial role in the formation and integration of sensory modalities during development. Postnatal behavior is thereby influenced by the type and timing of presentation of prenatal sensory stimuli. In this study, fertilized eggs of white Leghorn chickens during incubation were exposed to either species‐specific calls or no sound. To find the prenatal critical period when auditory stimulation can modulate visual system development, the former group was divided into three subgroups: in subgroup A (SGA), the stimulus was provided during embryonic day (E)10 to E16, in SGB E17‐ hatching, and in SGC E10‐hatching. The auditory and visual perceptual learning was recorded at posthatch day (PH) 1–3, whereas synaptic plasticity (evident from synaptophysin and PSD‐95 expression), was observed at E19, E20, and PH 1–3. An increased number of responders were observed in both auditory and visual preference tests at PH 1 following stimulation. Although a decrease in latency of entry and an increase in total time spent were observed in all stimulated groups, it was most significant in SGC in auditory preference and in SGB and SGC in visual preference test. The auditory cortex of SGC and visual Wulst of SGB and SGC revealed higher expression of synaptic proteins, compared to control and SGA. A significant inter‐hemispheric and gender‐based difference in expression was also found in all groups. These results indicate facilitation of postnatal behaviour and synaptogenesis in both auditory and visual systems following prenatal repetitive auditory stimulation, only when given during prenatal critical period of development. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 73: 688–701, 2013     

The effects of neck flexion on cerebral potentials evoked by visual,auditory and somatosensory stimuli and focal brain blood flow in related sensory cortices

Background

A flexed neck posture leads to non-specific activation of the brain. Sensory evoked cerebral potentials and focal brain blood flow have been used to evaluate the activation of the sensory cortex. We investigated the effects of a flexed neck posture on the cerebral potentials evoked by visual, auditory and somatosensory stimuli and focal brain blood flow in the related sensory cortices.

Methods

Twelve healthy young adults received right visual hemi-field, binaural auditory and left median nerve stimuli while sitting with the neck in a resting and flexed (20° flexion) position. Sensory evoked potentials were recorded from the right occipital region, Cz in accordance with the international 10–20 system, and 2 cm posterior from C4, during visual, auditory and somatosensory stimulations. The oxidative-hemoglobin concentration was measured in the respective sensory cortex using near-infrared spectroscopy.

Results

Latencies of the late component of all sensory evoked potentials significantly shortened, and the amplitude of auditory evoked potentials increased when the neck was in a flexed position. Oxidative-hemoglobin concentrations in the left and right visual cortices were higher during visual stimulation in the flexed neck position. The left visual cortex is responsible for receiving the visual information. In addition, oxidative-hemoglobin concentrations in the bilateral auditory cortex during auditory stimulation, and in the right somatosensory cortex during somatosensory stimulation, were higher in the flexed neck position.

Conclusions

Visual, auditory and somatosensory pathways were activated by neck flexion. The sensory cortices were selectively activated, reflecting the modalities in sensory projection to the cerebral cortex and inter-hemispheric connections.     

Multimodal spatial representations engaged in human parietal cortex during both saccadic and manual spatial orienting

BACKGROUND: Recent neuroimaging studies have found that several areas of the human brain, including parietal regions, can respond multimodally. But given single-cell evidence that responses in primate parietal cortex can be motor-related, some of the human multimodal activations might reflect convergent activation of potentially motor-related areas, rather than multimodal representations of space independent of motor factors. Here we crossed sensory stimulation of different modalities (vision or touch, in left or right hemifield) with spatially directed responses to such stimulation by different effector-systems (saccadic or manual). RESULTS: The fMRI results revealed representations of contralateral space in both the posterior part of the superior parietal gyrus and the anterior intraparietal sulcus that activated independently of both sensory modality and motor response. Multimodal saccade-related or manual-related activations were found, by contrast, in different regions of parietal cortex. CONCLUSIONS: Whereas some parietal regions have specific motor functions, others are engaged during the execution of movements to the contralateral hemifield irrespective of both input modality and the type of motor effector.     

Activation of Multimodal Areas in the Human Cerebral Cortex in Response to Biological Motion Sounds

Functional magnetic resonance imaging (fMRI) was used to investigate activation of the multimodal areas in the cerebral cortex–supramarginal and angular gyri, precuneus, and middle temporal visual cortex (MT/V5)–in response to motion of biologically significant sounds (human footsteps). The subjects listened to approaching or receding footstep sounds during 45 s, and such stimulation was supposed to evoke auditory adaptation to biological motion. Listening conditions alternated with stimulation-free control. To reveal activity in the regions of interest, the periods before and during stimulation were compared. Most stable and voluminous activation was detected in the supramarginal and angular gyri, being registered for all footstep sound types–approaching, receding and steps in place. Listening to human approaching steps activated the precuneus area, with the volume of activation clusters varying considerably between subjects. In the MT/V5 area, activation was revealed in 5 of 21 subjects. The involvement of the tested multimodal cortical areas in analyzing biological motion is discussed.     

Assessing visual requirements for social context-dependent activation of the songbird song system

Social context has been shown to have a profound influence on brain activation in a wide range of vertebrate species. Best studied in songbirds, when males sing undirected song, the level of neural activity and expression of immediate early genes (IEGs) in several song nuclei is dramatically higher or lower than when they sing directed song to other birds, particularly females. This differential social context-dependent activation is independent of auditory input and is not simply dependent on the motor act of singing. These findings suggested that the critical sensory modality driving social context-dependent differences in the brain could be visual cues. Here, we tested this hypothesis by examining IEG activation in song nuclei in hemispheres to which visual input was normal or blocked. We found that covering one eye blocked visually induced IEG expression throughout both contralateral visual pathways of the brain, and reduced activation of the contralateral ventral tegmental area, a non-visual midbrain motivation-related area affected by social context. However, blocking visual input had no effect on the social context-dependent activation of the contralateral song nuclei during female-directed singing. Our findings suggest that individual sensory modalities are not direct driving forces for the social context differences in song nuclei during singing. Rather, these social context differences in brain activation appear to depend more on the general sense that another individual is present.     

Prenatal music stimulation facilitates the postnatal functional development of the auditory as well as visual system in chicks (Gallus domesticus)

Rhythmic sound or music is known to improve cognition in animals and humans. We wanted to evaluate the effects of prenatal repetitive music stimulation on the remodelling of the auditory cortex and visual Wulst in chicks. Fertilized eggs (0 day) of white leghorn chicken (Gallus domesticus) during incubation were exposed either to music or no sound from embryonic day 10 until hatching. Auditory and visual perceptual learning and synaptic plasticity, as evident by synaptophysin and PSD-95 expression, were done at posthatch days (PH) 1, 2 and 3. The number of responders was significantly higher in the music stimulated group as compared to controls at PH1 in both auditory and visual preference tests. The stimulated chicks took significantly lesser time to enter and spent more time in the maternal area in both preference tests. A significantly higher expression of synaptophysin and PSD-95 was observed in the stimulated group in comparison to control at PH1-3 both in the auditory cortex and visual Wulst. A significant inter-hemispheric and gender-based difference in expression was also found in all groups. These results suggest facilitation of postnatal perceptual behaviour and synaptic plasticity in both auditory and visual systems following prenatal stimulation with complex rhythmic music.     

Basal forebrain cholinergic modulation of auditory activity in the zebra finch song system

The cholinergic basis of auditory "gating" in the sensorimotor nucleus HVc and its efferent target robustus archistriatalis (RA) was investigated in anesthetized zebra finches. Injections of cholinergic agonists carbachol or muscarine into HVc strongly affected discharge rates and diminished auditory responsiveness in both HVc and its target RA, changes toward an awake-like condition. HVc nicotine injections produced similar strong effects in HVc, but weaker and inconsistent effects in RA. Stimulation of basal forebrain (BF) produced an initial transient network shutdown followed by diminished auditory responsiveness in HVc and RA. All stimulation effects were blocked when preceded by HVc injections of nicotinic or muscarinic antagonists. Thus, BF cholinergic modulation of song system auditory activity acting via functionally distinct HVc circuits can contribute to auditory gating. We hypothesize that wakeful BF activity levels block sensory input to motor systems and adaptively change during behavior to allow sensorimotor feedback such as auditory feedback during singing.     

Role of sound stimulation in reprogramming brain connectivity

Sensory stimulation has a critical role to play in the development of an individual. Environmental factors tend to modify the inputs received by the sensory pathway. The developing brain is most vulnerable to these alterations and interacts with the environment to modify its neural circuitry. In addition to other sensory stimuli, auditory stimulation can also act as external stimuli to provide enrichment during the perinatal period. There is evidence that suggests that enriched environment in the form of auditory stimulation can play a substantial role in modulating plasticity during the prenatal period. This review focuses on the emerging role of prenatal auditory stimulation in the development of higher brain functions such as learning and memory in birds and mammals. The molecular mechanisms of various changes in the hippocampus following sound stimulation to effect neurogenesis, learning and memory are described. Sound stimulation can also modify neural connectivity in the early postnatal life to enhance higher cognitive function or even repair the secondary damages in various neurological and psychiatric disorders. Thus, it becomes imperative to examine in detail the possible ameliorating effects of prenatal sound stimulation in existing animal models of various psychiatric disorders, such as autism.     

Vestibular-Somatosensory Interactions: Effects of Passive Whole-Body Rotation on Somatosensory Detection

Vestibular signals are strongly integrated with information from several other sensory modalities. For example, vestibular stimulation was reported to improve tactile detection. However, this improvement could reflect either a multimodal interaction or an indirect interaction driven by vestibular effects on spatial attention and orienting. Here we investigate whether natural vestibular activation induced by passive whole-body rotation influences tactile detection. In particular, we assessed the ability to detect faint tactile stimuli to the fingertips of the left and right hand during spatially congruent or incongruent rotations. We found that passive whole-body rotations significantly enhanced sensitivity to faint shocks, without affecting response bias. Critically, this enhancement of somatosensory sensitivity did not depend on the spatial congruency between the direction of rotation and the hand stimulated. Thus, our results support a multimodal interaction, likely in brain areas receiving both vestibular and somatosensory signals.     

Does vestibular stimulation activate thalamocortical mechanisms that reintegrate impaired cortical regions?

Caloric stimulation induced a transient reversal of multimodal hemispatial cognitive deficits in an 81-year-old woman with an acute left cerebral hemisphere stroke. The patient had unawareness of her right hand (asomatognosia), right-sided visual unawareness (hemineglect), aphasia and right-sided weakness (hemiplegia) prior to the stimulation. Transient improvements in impaired sensory, motor, linguistic and cognitive function developed within 30 s following application of the caloric stimulus and onset of horizontal nystagmus. The effect persisted for 3 min and ceased completely after 5 min. While several recent reports have described the capacity of caloric stimulation to transiently improve or reverse a wide range of attentional, cognitive and motor impairments, most examples are in right-hemisphere-damaged patients with long-standing brain injury. Typically, patients have been tested several months or years after the onset of the deficit. A possible mechanism for the temporary reintegration of multiple cognitive functions in this patient is discussed.     

Sensory inputs stimulate progenitor cell proliferation in an adult insect brain

Although most brain neurons are produced during embryonic and early postnatal development, recent studies clearly demonstrated in a wide range of species from invertebrates to humans that new neurons are added to specific brain structures throughout adult life. Hormones, neurotransmitters, and growth factors as well as environmental conditions modulate this neurogenesis. In this study, we address the role of sensory inputs in the regulation of adult neural progenitor cell proliferation in an insect model. In some insect species, adult neurogenesis occurs in the mushroom bodies, the main sensory integrative centers of the brain, receiving multimodal information and often considered as the analog of the vertebrate hippocampus. We recently showed that rearing adult crickets in enriched sensory and social conditions enhanced neuroblast proliferation in the mushroom bodies. Here, by manipulating hormonal levels and affecting olfactory and/or visual inputs, we show that environmental regulation of neurogenesis is in direct response to olfactory and visual stimuli rather than being mediated via hormonal control. Experiments of unilateral sensory deprivation reveal that neuroblast proliferation can be inhibited in one brain hemisphere only. These results, obtained in a relatively simple brain, emphasize the role of sensory inputs on stem cell division.     

Tracking the mind's image in the brain I: time-resolved fMRI during visuospatial mental imagery

Mental imagery, the generation and manipulation of mental representations in the absence of sensory stimulation, is a core element of numerous cognitive processes. We investigate the cortical mechanisms underlying imagery and spatial analysis in the visual domain using event-related functional magnetic resonance imaging during the mental clock task. The time-resolved analysis of cortical activation from auditory perception to motor response reveals a sequential activation of the left and right posterior parietal cortex, suggesting that these regions perform distinct functions in this imagery task. This is confirmed by a trial-by-trial analysis of correlations between reaction time and onset, width, and amplitude of the hemodynamic response. These findings pose neurophysiological constraints on cognitive models of mental imagery.     

Postnatal changes in functional activities of the pig's brain: a combined functional magnetic resonance imaging and immunohistochemical study

Developmental changes in brain activation after pain stimulation and after passive movement of the hind paw were assessed by functional magnetic resonance imaging (fMRI) in pigs of postnatal ages 2, 4 and 6 months. Response patterns were correlated with histological maturation parameters. At 2 months, fMRI failed to detect brain activation after pain stimulation and revealed weak, but widespread activation after passive movement. At 4 months, strong reaction of numerous cortical areas on the contralateral side was seen after pain stimulation. Following passive movement, activation was weaker but more widespread, and the brainstem was also involved. By 6 months, cortical activation became more restricted to the contralateral sensory cortex and brainstem after pain stimulation and to the contralateral sensory and ipsilateral premotor and motor cortices after passive movement. Neocortical synaptophysin immunoreaction increased significantly between 2 and 4 months and slightly decreased by 6 months. The density of GABA-immunoreactive neurons and fibers significantly increased, reaching a maximum at 6 months. Our studies indicate that remodeling of synapses and development of inhibitory GABA neurons last until 6 months postnatally, when the fMRI response of the pig's brain also attains its mature adult pattern.     

Selective attention and memory: evoked potentials in visual and auditory verbal competition

The brain mechanisms of the selective verbal attention were studied using evoked potential (EP) technique. It was shown that the late "cognitive" EP components (400-800 ms) related to memory function were more positive to the words presented via a relevant sensory channel and more negative to irrelevant words. The hypothesis is advanced that words delivered via two competing sensory channels, such as visual and auditory, are perceived, i.e., the subject sees and hears them. However, irrelevant signals are not stored in episodic memory due to the active inhibition of the information transmission to the hippocampal structures.     

Effects of Multimodal Load on Spatial Monitoring as Revealed by ERPs

While the role of selective attention in filtering out irrelevant information has been extensively studied, its characteristics and neural underpinnings when multiple environmental stimuli have to be processed in parallel are much less known. Building upon a dual-task paradigm that induced spatial awareness deficits for contralesional hemispace in right hemisphere-damaged patients, we investigated the electrophysiological correlates of multimodal load during spatial monitoring in healthy participants. The position of appearance of briefly presented, lateralized targets had to be reported either in isolation (single task) or together with a concurrent task, visual or auditory, which recruited additional attentional resources (dual-task). This top-down manipulation of attentional load, without any change of the sensory stimulation, modulated the amplitude of the first positive ERP response (P1) and shifted its neural generators, with a suppression of the signal in the early visual areas during both visual and auditory dual tasks. Furthermore, later N2 contralateral components elicited by left targets were particularly influenced by the concurrent visual task and were related to increased activation of the supramarginal gyrus. These results suggest that the right hemisphere is particularly affected by load manipulations, and confirm its crucial role in subtending automatic orienting of spatial attention and in monitoring both hemispaces.     

节律性听觉刺激下的神经振荡同步化及其应用

大脑的感觉、情绪、认知等功能与其神经振荡模式有密切的联系。通过施加节律性刺激可以调控大脑的神经振荡模式,进而影响个体感受、情绪状态和认知功能等。与近年来常见的非侵入性电刺激和磁刺激相比,同样依赖于外部刺激输入的节律性感觉刺激具有成本低、易操作等优点,被认为是一种极具潜力的神经调控手段。本文以节律性听觉刺激为例,系统综述了不同类型的节律性听觉刺激如何影响大脑的神经振荡模式,进而影响相关状态和功能;并通过总结外部节律性听觉刺激对个体感知觉、情绪与认知功能的影响,讨论其生理机制和应用前景。     

Effects of aerobic exercise and gender on visual and auditory P300, reaction time, and accuracy

Visual and auditory reaction times (RTs) have been reported to decrease during moderate aerobic exercise, and this has been interpreted as reflecting an exercise-induced activation (EIA) of cognitive information processing. In the present study we examined changes in several independent measures of information processing (RT, accuracy, P300 latency and amplitude) during exercise, and their relationship to visual or auditory modalities and to gender. P300 latencies offer independent measures of cognitive speed that are unrelated to motor output, and P300 amplitudes have been used as measures of attentional allocation. Twenty-four healthy college students [mean (SD) age 20 (2) years] performed auditory and visual "oddball" tasks during resting baseline, aerobic exercise, and recovery periods. Consistent with previous studies, both visual and auditory RTs during exercise were significantly shortened compared to control and recovery periods (which did not differ from each other). We now report that, paralleling the RT changes, auditory and visual P300 latencies decreased during exercise, indicating the occurrence of faster cognitive information processing in both sensory modalities. However, both auditory and visual P300 amplitudes decreased during exercise, suggesting diminished attentional resource allocation. In addition, error rates increased during exercise. Taken together, these results suggest that the enhancement of cognitive information processing speed during moderate aerobic exercise, although operating across genders and sensory modalities, is not a global facilitation of cognition, but is accompanied by decreased attention and increased errors.     

Rapid Changes in Cortical and Subcortical Brain Regions after Early Bilateral Enucleation in the Mouse

Functional sensory and motor areas in the developing mammalian neocortex are formed through a complex interaction of cortically intrinsic mechanisms, such as gene expression, and cortically extrinsic mechanisms such as those mediated by thalamic input from the senses. Both intrinsic and extrinsic mechanisms are believed to be involved in cortical patterning and the establishment of areal boundaries in early development; however, the nature of the interaction between intrinsic and extrinsic processes is not well understood. In a previous study, we used a perinatal bilateral enucleation mouse model to test some aspects of this interaction by reweighting sensory input to the developing cortex. Visual deprivation at birth resulted in a shift of intraneocortical connections (INCs) that aligned with ectopic ephrin A5 expression in the same location ten days later at postnatal day (P) 10. A prevailing question remained: Does visual deprivation first induce a change in gene expression, followed by a shift in INCs, or vice versa? In the present study, we address this question by investigating the neuroanatomy and patterns of gene expression in post-natal day (P) 1 and 4 mice following bilateral enucleation at birth. Our results demonstrate a rapid reduction in dorsal lateral geniculate nucleus (dLGN) size and ephrin A5 gene expression 24-hours post-enucleation, with more profound effects apparent at P4. The reduced nuclear size and diminished gene expression mirrors subtle changes in ephrin A5 expression evident in P1 and P4 enucleated neocortex, 11 and 8 days prior to natural eye opening, respectively. Somatosensory and visual INCs were indistinguishable between P1 and P4 mice bilaterally enucleated at birth, indicating that perinatal bilateral enucleation initiates a rapid change in gene expression (within one day) followed by an alteration of sensory INCs later on (second postnatal week). With these results, we gain a deeper understanding of how gene expression and sensory input together regulate cortical arealization and plasticity during early development.     

Sensory projections to the cerebral cortex inPerodicticus potto edwarsi Bouvier

The cortical sensory projections of somatic, auditory, and visual origin have been mapped in the chloralosed potto. The pathways of the contralateral side of the body project in a classical somatotopic fashion to a large area SI, behind the motor cortex and the central sulcus. The latter constitutes the posterior boundary of the motor cortex only in its ventral part. In its middle zone the motor cortex extends to its posterior lip. Above the sulcus the motor zone is immediately adjacent to the preparietal area. Visual evoked potentials are recorded behind the transverse occipital sulcus with a maximal focus just caudal to an occipital dimple. The auditory area is situated between the sylvian and parallel sulci. No heterosensory potentials (visual or auditory) can be recorded from the somatomotor area, nor from any other part outside their primary projection area. An area of convergent somatic projection devoid of somatotopic organization is found between SI and the auditory zone and another one in front of the central sulcus. In view of the poor cortical heterosensory integration, the sensory projection system of the potto seems to be less developed than in the cat.     

Auditory Evoked Bursts in Mouse Visual Cortex during Isoflurane Anesthesia

General anesthesia is not a uniform state of the brain. Ongoing activity differs between light and deep anesthesia and cortical response properties are modulated in dependence of anesthetic dosage. We investigated how anesthesia level affects cross-modal interactions in primary sensory cortex. To examine this, we continuously measured the effects of visual and auditory stimulation during increasing and decreasing isoflurane level in the mouse visual cortex and the subiculum (from baseline at 0.7 to 2.5 vol % and reverse). Auditory evoked burst activity occurred in visual cortex after a transition during increase of anesthesia level. At the same time, auditory and visual evoked bursts occurred in the subiculum, even though the subiculum was unresponsive to both stimuli previous to the transition. This altered sensory excitability was linked to the presence of burst suppression activity in cortex, and to a regular slow burst suppression rhythm (∼0.2 Hz) in the subiculum. The effect disappeared during return to light anesthesia. The results show that pseudo-heteromodal sensory burst responses can appear in brain structures as an effect of an anesthesia induced state change.