Effects of aging on peripheral and central auditory processing in rats.

Hearing loss is a hallmark sign in the elderly population. Decline in auditory perception provokes deficits in the ability to localize sound sources and reduces speech perception, particularly in noise. In addition to a loss of peripheral hearing sensitivity, changes in more complex central structures have also been demonstrated. Related to these, this study examines the auditory directional maps in the deep layers of the superior colliculus of the rat. Hence, anesthetized Sprague-Dawley adult (10 months) and aged (22 months) rats underwent distortion product of otoacoustic emissions (DPOAEs) to assess cochlear function. Then, auditory brainstem responses (ABRs) were assessed, followed by extracellular single-unit recordings to determine age-related effects on central auditory functions. DPOAE amplitude levels were decreased in aged rats although they were still present between 3.0 and 24.0 kHz. ABR level thresholds in aged rats were significantly elevated at an early (cochlear nucleus - wave II) stage in the auditory brainstem. In the superior colliculus, thresholds were increased and the tuning widths of the directional receptive fields were significantly wider. Moreover, no systematic directional spatial arrangement was present among the neurons of the aged rats, implying that the topographical organization of the auditory directional map was abolished. These results suggest that the deterioration of the auditory directional spatial map can, to some extent, be attributable to age-related dysfunction at more central, perceptual stages of auditory processing.

Temporary deafness can impair multisensory integration: a study of cochlear-implant users.

Previous investigations suggest that temporary deafness can have a dramatic impact on audiovisual speech processing. The aim of this study was to test whether temporary deafness disturbs other multisensory processes in adults. A nonspeech task involving an audiotactile illusion was administered to a group of normally hearing individuals and a group of individuals who had been temporarily auditorily deprived. Members of this latter group had their auditory detection thresholds restored to normal levels through the use of a cochlear implant. Control conditions revealed that auditory and tactile discrimination capabilities were identical in the two groups. However, whereas normally hearing individuals integrated auditory and tactile information, so that they experienced the audiotactile illusion, individuals who had been temporarily deprived did not. Given the basic nature of the task, failure to integrate multisensory information could not be explained by the use of the cochlear implant. Thus, the results suggest that normally anticipated audiotactile interactions are disturbed following temporary deafness.

Development of the representation of auditory space in the superior colliculus of the rat.

The aims of the present study were, first, to determine the time of the emergence of the topographic map in the superior colliculus (SC) of the rat and, second, to examine the spatial changes in auditory neurons' receptive fields (RFs) throughout the developmental period. For these purposes, recording sessions were conducted on rats of different age groups (P15-18; P21-24; P27-29 and P60-80). Results show that SC auditory neurons' RFs go through multiple changes during early development before the establishment of the adult-like auditory topographic map (P27). These modifications include, first, the refining of directional RFs tuning between P18 and P27 and, second, a shift of sensitivity towards 90 degrees in the contralateral hemispace after P15-18. In addition, data indicate that the neuronal response latencies are shorter in the adult group than in the P15-18 or P21-24 groups. Finally, a diminution in spontaneous firing rate was observed between the P15-18 group and the P60-80 group. The results of the present study revealed that the neural organization representing auditory space in the deep layers of the SC of the rat is not innate, but rather emerges at about P27-29. Moreover, they bring new evidence supporting a two-step process involved in the development of the representation of auditory space. Hence, the development of the auditory space representation follows a logical temporal maturation sequence whereby the RF organization must be completed before a stable topographic map can be formed.

Global motion stimuli and form-from-motion stimuli: common characteristics and differential activation patterns.

We used functional Magnetic Resonance Imaging (fMRI) to explore the areas underlying the processing of two similar motion stimuli that evoke different types of processing. The results indicated that while form-from-motion (FFM) stimuli activated both lateral occipital complex (LOC) and MT complex (MT+), only the LOC remained significantly activated when contrasted with a global motion stimulus (GMS) with different coherence levels. Because of the large number of common characteristics shared between the stimuli, this contrast enabled us to isolate the regions implicated in form processing. The GMS on the other hand only activated MT+, reaching maximal intensity for low coherence. Overall, these data illustrate how two similar motion stimuli can elicit the participation of different cortical visual regions.

Effects of early binocular enucleation on auditory and somatosensory coding in the superior colliculus of the rat.

The present study aimed at investigating the effects of early visual deprivation (bilateral neonatal enucleation) on auditory and somatosensory coding in the polysensory deep layers of the superior colliculus of the rat. The proportion of cells responding to auditory and somatosensory stimulation and the receptive field properties of single neurons were assessed in both normal and enucleated rats. As expected, in enucleated rats there was a drastic increase in the number of unresponsive units and visual responses could no longer be evoked. Most importantly, the proportion of cells that responded to auditory stimulation was drastically reduced. However, the few cells that remained responsive to auditory stimulation were well tuned to noise stimuli presented in both azimuth and elevation, principally in the contralateral hemifield. Enucleation also increased the proportion of cells responding to somatosensory stimulation, particularly to the vibrissae. Implications in terms of neural plasticity and functionality are discussed.

Early- and late-onset blind individuals show supra-normal auditory abilities in far-space.

Blind individuals manifest remarkable abilities in navigating through space despite their lack of vision. They have previously been shown to perform normally or even supra-normally in tasks involving spatial hearing in near space, a region that, however, can be calibrated with sensory-motor feedback. Here we show that blind individuals not only properly map auditory space beyond their peri-personal environment but also demonstrate supra-normal performance when subtle acoustic cues for target location and distance must be used to carry out the task. Moreover, it is generally postulated that such abilities rest in part on cross-modal cortical reorganizations, particularly in the immature brain, where important synaptogenesis is still possible. Nonetheless, we show for the first time that even late-onset blind subjects develop above-normal spatial abilities, suggesting that significant compensation can occur in the adult.

Enhancement of sound motion detection in acallosal individuals.

It has been proposed that the corpus callosum may play an important role in spectral cue processing that allows vertical auditory movement perception. The purpose of the present study was to assess the contribution of the corpus callosum to this type of auditory processing. Noise bursts were presented to 10 control and two callosal agenesis individuals from different positions located within midsagittal and coronal planes. Although acallosal participants were comparable with controls in their ability to correctly identify the trajectory direction or its length, they showed greater capability in detecting motion per se when the task was difficult. These results suggest that in the absence of the corpus callosum, compensatory reorganization of the brain allowed for superior auditory spectral cue processing.

Spatio-temporal receptive field properties of cells in the rat superior colliculus.

Although the rat is widely used in neurobehavioural research, the spatio-temporal receptive field properties of neurons in superficial layers of the superior colliculus are relatively unknown. Extracellular recordings were carried out in anesthetized Long Evans rats. Neurons in these layers had simple-like and complex-like receptive fields (RFs). Most cells (67%) had RFs showing band-pass and low-pass spatial frequency (SF) tuning profiles. Spatial band-pass profiles showed low optimal SF (mean=0.03 c/deg), low spatial resolution (mean=0.18 c/deg) and large spatial bandwidths (mean=2.3 octaves). More than two-thirds of the RFs (71%) were selective to orientation and only 11% were clearly direction selective. Nearly two-thirds of cells (68%) had band-pass temporal frequency (TF) tuning profiles with narrow bandwidths (mean=1.7 oct.) whereas the others showed low-pass TF tuning profiles. Temporal band-pass profiles had low optimal TFs (mean=3.5 c/s). Although some cells showed relatively low contrast thresholds (6%), most cells only responded to high contrast values (mean=38.2%). These results show that the spatial resolution of collicular cells is poor and that they respond mainly to highly contrasted moving stimuli.

Spectral and temporal auditory processing in the superior colliculus of aged rats.

Presbyacusis reflects dysfunctions present along the central auditory pathway. Given that the topographic representation of the auditory directional spatial map is deteriorated in the superior colliculus of aged animals, therefore, are spectral and temporal auditory processes altered with aging in the rat's superior colliculus? Extracellular single-unit recordings were conducted in the superior colliculus of anesthetized Sprague-Dawley adult (10 months) and aged (22 months) rats. In the spectral domain, level thresholds in aged rats were significantly increased when superior colliculus auditory neurons were stimulated with pure tones or Gaussian noise bursts. The sharpness of the frequency response tuning curve at 10 dB SPL above threshold was also significantly broader among the aged rats. Furthermore, in the temporal domain, the minimal silent gap thresholds to Gaussian noises were significantly longer in aged rats. Hence, these results highlight that spectral and temporal auditory processing in the superior colliculus are impaired during aging.

Systemic blood pressure alters cortical blood flow and neurovascular coupling during nociceptive processing in the primary somatosensory cortex of the rat.

Inference on nociceptive and pain-related processes from functional magnetic resonance imaging is made with the assumption that the coupling of neuronal activity and cerebral hemodynamic changes is stable. However, since nociceptive stimulation is associated with increases in systemic arterial pressure, it is essential to determine whether this coupling remains the same during different levels of nociception and pain. The main objective of the present study was to compare the amplitude of local field potentials (LFP) and cerebral blood flow (CBF) changes in the primary somatosensory cortex during nociceptive electrical stimulation of the contralateral or ipsilateral forepaw in isoflurane-anesthetized rats, while manipulating mean arterial pressure (MAP). MAP changes induced by nociceptive stimulation were manipulated by transecting the spinal cord at the upper thoracic segments (T1-T2), which interrupts sympathetic pathways and prevents nociception-related MAP increases, while sensory pathways between the forepaws and the brain remain intact. Intensity-dependent increases in MAP and CBF were observed and these effects were abolished or significantly decreased after spinal transection (p<0.001 and p<0.05, respectively). In contrast, the intensity-dependent changes in LFP amplitude were decreased for the contralateral stimulation but increased for the ipsilateral stimulation after spinal transection (p<0.05). Thus, neurovascular coupling was altered differently by stimulus-induced MAP changes, depending on stimulus intensity and location. This demonstrates that CBF changes evoked by nociceptive processing do not always match neuronal activity, which may lead to inaccurate estimation of neuronal activity from hemodynamic changes. These results have important implications for neuroimaging of nociceptive and pain-related processes.

Development of visual-evoked potentials to radially modulated concentric patterns.

The visual processing of radially modulated concentric patterns was studied in human participants, aged 3-22 years, by recording event-related potentials. These stimuli are known to activate the fusiform face area as well as area V4 in normal adults. The electrophysiological data showed a P1 latency that reached a maturation asymptote before 3 years of age, whereas that of N1 and P2 became adultlike by 13 years of age. In addition, the distribution of the P2 component over the scalp was focalized in the primary visual cortex before adolescence and became distributed over the entire brain after adolescence. Radially modulated concentric stimuli thus induce brain activation that is not mature until 13 years of age.

Effective binocular integration at the midline requires the corpus callosum.

To study the role of the corpus callosum (CC) in midline binocular integration, the effects of late callosotomy and congenital CC agenesis on the ability to perceive dichoptic plaid motion was assessed. Coherent motion was well perceived at all locations in the visual field under dioptic viewing but not along the vertical meridian (VM) when the components were dichoptically presented. This deficit was totally abolished in the agenesis subject and reduced in the callosotomized individual when stimulus size was increased beyond the VM. Electrophysiological correlates were also examined by recording visual evoked potentials and these showed that the P1/N2 components were abnormal for small dichoptic stimuli presented on the midline. These findings attest to the importance of the contribution of CC to midline binocular integration and the effects of cerebral plasticity.

Phase disparity in area 19 of the cat.

Binocular cells in area 19 are tuned to positional disparities. In effect, up to one-third of the cells respond preferentially to small incongruities between the optimal bar stimuli presented within the receptive fields of each eye. The aim of the present study was to determine whether cells in area 19 are also sensitive to phase disparities. Both types of disparities have been proposed as mechanisms through which stereoperception is achieved. Results indicate that phase disparities produced coherent interactions in 38% of the binocular cells, resulting in facilitation or summation. The remaining cells were phase insensitive. The overall results suggest that cells in area 19 code phase disparities in a proportion comparable to stimulus disparities, confirming that this area is implicated in binocular integration, albeit in a relatively smaller proportion than some of the other visual areas.

Disparity sensitivity in the superior colliculus of the cat.

The present study aims at evaluating the spatial disparity response profiles of binocular cells in the superficial layers of the superior colliculus of the cat using drifting light bars and phase-shifted spatial frequency gratings. Results show that a total of 64% of the cells were sensitive to phase disparities and had large tuning profiles. Similarly, a large proportion (75%) of those tested with position offsets showed one of the four classic disparity profiles, those of the tuned cells being rather coarse. When tested with both position and phase disparities, 54% of the cells showed sensitivity profiles to the two types of stimuli. The overall results suggest that the superior colliculus is involved in the analysis of coarse stereopsis and/or the planning and initiation of saccades during vergence eye movements and/or the control of fine adjustments to maintain fixation as the stimulus moves in depth.

Influence of NO downregulation on oscillatory evoked responses in developing rat superior colliculus.

Nitric oxide (NO) is involved in neuronal transmission by modulating neurotransmitter release in adults and in stabilizing synaptic connections in developing brains. We investigated the influence of downregulation of NO synthesis on oscillatory components of ON and OFF evoked field potentials in the rat superior colliculus. NO synthesis was decreased by inhibiting nitric oxide synthase (NOS) with an acute microinjection of N(omega)-nitro-L-arginine methyl ester (L-NAME). The study focuses on rhythmic activity by analyzing fast Fourier transform (FFT). Collicular responses were recorded in anesthetized rats, at postnatal days (PND) 13-19 and adults. This time window was chosen because it is centered on eye opening. NO downregulation resulted in a dual effect depending on age and response-type. NO synthesis inhibition decreased the magnitude of oscillations in ON responses in the youngest animals (PND13-14), whereas oscillations of frequencies higher than 20 Hz in OFF responses were increased in all age groups of developing rats. In adults NO downregulation increased oscillations in ON responses and decreased oscillations in OFF responses. L-Arginine was used to increase NOS activity and its injection produced effects opposite to those seen with L-NAME. Slow oscillatory components (7-12 Hz) were unaffected in all experiments. Our data together with results reported in the literature suggest that rhythmic patterns of activity are NO-dependent.

Audiotactile interaction can change over time in cochlear implant users.

Recent results suggest that audiotactile interactions are disturbed in cochlear implant (CI) users. However, further exploration regarding the factors responsible for such abnormal sensory processing is still required. Considering the temporal nature of a previously used multisensory task, it remains unclear whether any aberrant results were caused by the specificity of the interaction studied or rather if it reflects an overall abnormal interaction. Moreover, although duration of experience with a CI has often been linked with the recovery of auditory functions, its impact on multisensory performance remains uncertain. In the present study, we used the parchment-skin illusion, a robust illustration of sound-biased perception of touch based on changes in auditory frequencies, to investigate the specificities of audiotactile interactions in CI users. Whereas individuals with relatively little experience with the CI performed similarly to the control group, experienced CI users showed a significantly greater illusory percept. The overall results suggest that despite being able to ignore auditory distractors in a temporal audiotactile task, CI users develop to become greatly influenced by auditory input in a spectral audiotactile task. When considered with the existing body of research, these results confirm that normal sensory interaction processing can be compromised in CI users.

Neurovascular coupling during nociceptive processing in the primary somatosensory cortex of the rat.

Neuroimaging methods such as functional magnetic resonance imaging (fMRI) have been used extensively to investigate pain-related cerebral mechanisms. However, these methods rely on a tight coupling of neuronal activity to hemodynamic changes. Because pain may be associated with hemodynamic changes unrelated to local neuronal activity (eg, increased mean arterial pressure [MAP]), it is essential to determine whether the neurovascular coupling is maintained during nociceptive processing. In this study, local field potentials (LFP) and cortical blood flow (CBF) changes evoked by electrical stimulation of the left hind paw were recorded concomitantly in the right primary somatosensory cortex (SI) in 15 rats. LFP, CBF, and MAP changes were examined in response to stimulus intensities ranging from 3 to 30 mA. In addition, LFP, CBF, and MAP changes evoked by a 10-mA stimulation were examined during immersion of the tail in non-nociceptive or nociceptive hot water (counter-stimulation). SI neurovascular coupling was altered for stimuli of nociceptive intensities (P<0.001). This alteration was intensity-dependent and was strongly associated with MAP changes (r=0.98, P<0.001). However, when the stimulus intensity was kept constant, SI neurovascular coupling was not significantly affected by nociceptive counter-stimulation (P=0.4), which similarly affected the amplitude of shock-evoked LFP and CBF changes. It remains to be determined whether such neurovascular uncoupling occurs in humans, and whether it also affects other regions usually activated by painful stimuli. These results should be taken into account for accurate interpretation of fMRI studies that involve nociceptive stimuli associated with MAP changes.

Cortical development of the visual system of the rat.

Although rat is commonly used for studying the visual system, the development of spatio-temporal receptive field properties of neurons in its primary visual cortex remains relatively unknown. Extracellular single neuron recordings were thus carried out in anaesthetized newborn rats between postnatal (P) day 15 and 30 and in adult rats. The first neuronal responses evoked by drifting sinusoidal gratings were obtained at P16. From P27-P30 to adulthood, the neurons' optimal temporal frequency significantly increased, whereas the contrast threshold decreased. However, the optimal spatial frequency, spatial resolution and spatial bandwidth were, soon after eye opening, similar to those observed in the adult rat. The differential maturation of receptive field properties is discussed with regard to the functional pathways of the rat visual system.

Coding sound direction in noisy environment in the superior colliculus of the rat.

The aim of the present study was to evaluate the effect of background noise on the directional sensitivity of neurons in the deep layers of the superior colliculus. Extra-cellular recordings were carried out in anaesthetized adult Long Evans rats. When stimulated in a noisy environment, most of the neurons remained sensitive to sound direction and only a few changed their optimal direction by more than 15 degrees. When stimulated at their optimal direction in the presence of background noise, a majority of neurons did not modify their response rate, whereas a limited proportion of neurons showed either a significant drop or facilitation of their response rate. Moreover, the neurons' receptive fields showed significant tuning modifications in the presence of background noise. In a noisy environment, the larger receptive fields became narrower, whereas the sharply tuned receptive fields got broader.

Visual deprivation modifies auditory directional tuning in the inferior colliculus.

The aim of this study was to assess whether early visual deprivation could modulate the auditory directional tunings of single neurons in the central nucleus of the inferior colliculus of the rat. Extracellular recordings were carried out in normal and early bilaterally enucleated rats. Direction-specific auditory neurons were found in both groups, and no evidence was found for a topographical order of best azimuthal direction. Although the distribution of best azimuthal direction was unaltered in enucleated rats, our data suggest that early visual deprivation modifies the width of auditory directional receptive fields in the central nucleus of the inferior colliculus. This suggests that visual input plays a substantial role in refining auditory receptive fields in the inferior colliculus.