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Orienting responses to a sound before and after (i) and during (ii) unilateral deactivation of 4 polysensory areas: vPE (A; 4 hemispheres in 2 cats), dPE (B; 6 hemispheres in 4 cats), 7a (C; 8 hemispheres in 4 cats), and 7p (D; 4 hemispheres in 2 cats). For conventions, see Fig. 4.
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We examined the ability of mature cats to accurately orient to, and approach, an acoustic stimulus during unilateral reversible cooling deactivation of primary auditory cortex (AI) or 1 of 18 other cerebral loci. After attending to a central visual stimulus, the cats learned to orient to a 100-ms broad-band, white-noise stimulus emitted from a cent...
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The brain integrates information from multiple sensory modalities and, through this process, generates a coherent and apparently seamless percept of the external world. Although multisensory integration typically binds information that is derived from the same event, when multisensory cues are somewhat discordant they can result in illusory percept...
Previous ERP studies have uncovered cross-modal interactions in endogenous spatial attention. Directing attention to one side to judge stimuli from one particular modality can modulate early modality-specific ERP components not only for that modality, but also for other currently irrelevant modalities. However, past studies could not determine whet...
Citations
... On each trial, one of the eight speakers (the "goal") played a continuous stream of intermittent noise bursts. The auditory stimulus continued throughout the entire trial until the mouse poked the correct port (Fig 1D), in contrast to typical auditory localization tasks that use a single brief stimulus (Kavanagh and Kelly, 1987;Recanzone et al., 2000;Malhotra, Hall and Lomber, 2004;Kacelnik et al., 2006;Van Bentum, Van Opstal and Van Wanrooij, 2021;Town and Bizley, 2022). The mouse received a reward for poking the port below the goal speaker. ...
How we move our bodies affects how we perceive sound. For instance, we can explore an environment to seek out the source of a sound and we can use head movements to compensate for hearing loss. How we do this is not well understood because many auditory experiments are designed to limit head and body movements. To study the role of movement in hearing, we developed a behavioral task called sound-seeking that rewarded mice for tracking down an ongoing sound source. Over the course of learning, mice more efficiently navigated to the sound. We then asked how auditory behavior was affected by hearing loss induced by surgical removal of the malleus from the middle ear. An innate behavior, the auditory startle response, was abolished by bilateral hearing loss and unaffected by unilateral hearing loss. Similarly, performance on the sound-seeking task drastically declined after bilateral hearing loss and did not recover. In striking contrast, mice with unilateral hearing loss were only transiently impaired on sound-seeking; over a recovery period of about a week, they regained high levels of performance, increasingly reliant on a different spatial sampling strategy. Thus, even in the face of permanent unilateral damage to the peripheral auditory system, mice recover their ability to perform a naturalistic sound-seeking task. This paradigm provides an opportunity to examine how body movement enables better hearing and resilient adaptation to sensory deprivation.
... A head holder was attached to the frontal bone of the skull using bone screws and dental acrylic. The animal was then provided with standard postoperative care (see Malhotra et al., 2004). In all cases, recovery was uneventful. ...
Many neural areas, where patterned activity is lost following deafness, have the capacity to become activated by the remaining sensory systems. This crossmodal plasticity can be measured at perceptual/behavioural as well as physiological levels. The dorsal zone (DZ) of auditory cortex of deaf cats is involved in supranormal visual motion detection, but its physiological level of crossmodal reorganisation is not well understood. The present study of early-deaf DZ (and hearing controls) used multiple single-channel recording methods to examine neuronal responses to visual, auditory, somatosensory and combined stimulation. In early-deaf DZ, no auditory activation was observed, but 100% of the neurons were responsive to visual cues of which 21% were also influenced by somatosensory stimulation. Visual and somatosensory responses were not anatomically organised as they are in hearing cats, and fewer multisensory neurons were present in the deaf condition. These crossmodal physiological results closely correspond with and support the perceptual/behavioural enhancements that occur following hearing loss.
... Both hemispheres are necessary for an effective sound localization. Lesion studies often indicate contralateral localization deficits after unilateral lesions [30][31][32][33], indicating that one hemisphere is sufficient to precisely localize sounds in the contralateral region. On the other hand, studies on sound localization frequently report more precise location estimations when integrating input from different hemispheres [34][35][36], showing that combining information from bilateral auditory cortices is ideal. ...
... In addition, location-specific VASI accuracy score results indicated that the right dominant group had a better score in the left spatial location and left dominant group acheived better score in right spatial location, owing to the fact of contralateral neural connection of nervous system [43][44][45]. This also corelates with lesion studies indicating contralateral localization deficits after unilateral lesions [30][31][32][33]. MANOVA results for location-specific VASI scores showed that VASI accuracy at 0, 180, R 90 and L 90 are not influenced by cerebral dominance. ...
Background. Cerebral dominance refers to the biological description of the brain, where one cerebral hemisphere is dominant over the other in certain cerebral functions. There is scanty literature on cerebral dominance and its impact on auditory spatial processing and working memory, which is explored in the study. Methods A total of 45 participants with normal hearing were divided into three groups of 15 participants. The groups were categorized based on scores obtained on the alert scale of the cognitive style checklist as the bilateral dominant, left dominant, and the right dominant group. The spatial hearing was assessed using interaural time difference (ITD), the interaural level difference (ILD), and virtual acoustic space identification (VASI) tests, whereas the auditory working memory abilities were tested using forward span, backward span, ascending digit span, descending digit span, and 2n back tests. Results MONOVA results indicated that there is no significant main effect of cerebral dominance on all auditory working memory tests. In spatial hearing, although ILD and ILD thresholds were not influenced by cerebral dominance, the main effect of cerebral dominance was seen on VASI accuracy scores. Post-hoc analyses of VASI scores showed that the bilateral dominant group demonstrated significantly better spatial perception scores compared to the left and right dominant groups, with latter groups showing similar performance. Conclusions While ITD and ILD tests fall short of revealing cerebral asymmetry, VASI’s power in capturing cerebral dominance effects makes it a valuable tool in spatial processing assessment. The study’s findings highlight the need for assessing cerebral dominance, before administering spatial hearing tests.
Keywords Cerebral dominance, Working memory, Spatial hearing, Virtual auditory space identification test, Dominant-brain
... Considering permanent lesion or reversible deactivation studies, cat area 5 and part of area 6 have been found to be essential for the action of orientation behavior, as their deactivation eliminates both acoustic and visual localization (Malhotra et al., 2004). Some other areas are essential for acoustic-specific orientation, such as the primary auditory cortex, PAF, and anterior ectosylvian sulcus (AES) (Malhotra et al., 2004). ...
... Considering permanent lesion or reversible deactivation studies, cat area 5 and part of area 6 have been found to be essential for the action of orientation behavior, as their deactivation eliminates both acoustic and visual localization (Malhotra et al., 2004). Some other areas are essential for acoustic-specific orientation, such as the primary auditory cortex, PAF, and anterior ectosylvian sulcus (AES) (Malhotra et al., 2004). Areas such as the posterior middle suprasylvian sulcus (pMS), dorsal posterior ectosylvian gyrus (dPE), and posterior suprasylvian sulcus (PS) are critical for visual orientation (Lomber and Payne, 2004). ...
... The deactivation of deaf PAF eliminated the improved performance in the peripheral visual field (Lomber et al., 2010), which suggests that neurons in PAF acquire some functions in visual representations and/or motor planning. While there is still no evidence of visual responsiveness of PAF neurons in either hearing or deaf cats, cortical deactivation experiments show that PAF in hearing animals is involved in auditory localization (Malhotra et al., 2004;Malhotra and Lomber, 2007) and that PAF neurons are better tuned for sound location than A1 or AAF (Harrington et al., 2008). Therefore, neurons in PAF in hearing cats may already carry information of space required for the motor planning in visually guided orienting behavior, and may acquire functions in processing visual inputs following deafness. ...
Introduction
Congenitally deaf cats perform better on visual localization tasks than hearing cats, and this advantage has been attributed to the posterior auditory field. Successful visual localization requires both visual processing of the target and timely generation of an action to approach the target. Activation of auditory cortex in deaf subjects during visual localization in the peripheral visual field can occur either via bottom-up stimulus-driven and/or top-down goal-directed pathways.
Methods
In this study, we recorded visually evoked potentials (VEPs) in response to a reversing checkerboard stimulus presented in the hemifield contralateral to the recorded hemisphere in both hearing and deaf cats under light anesthesia.
Results
Although VEP amplitudes and latencies were systematically modulated by stimulus eccentricity, we found little evidence of changes in VEP in deaf cats that can explain their behavioral advantage. A statistical trend was observed, showing larger peak amplitudes and shorter peak latencies in deaf subjects for stimuli in the near- and mid-peripheral field. Additionally, latency of the P1 wave component had a larger inter-sweep variation in deaf subjects.
Discussion
Our results suggested that cross-modal plasticity following deafness does not play a major part in cortical processing of the peripheral visual field when the “vision for action” system is not recruited.
... A head holder was attached to the frontal bone of the skull using bone screws and dental acrylic. The animal was then provided with standard postoperative care (see Malhotra et al. 2004). In all cases, recovery was uneventful. ...
From myriads of ongoing stimuli, the brain creates a fused percept of the environment. This process, which culminates in perceptual binding, is presumed to occur through the operations of multisensory neurons that occur throughout the brain. However, because different brain areas receive different inputs and have different cytoarchitechtonics, it would be expected that local multisensory features would also vary across regions. The present study investigated that hypothesis using multiple single-unit recordings from anesthetized cats in response to controlled, electronically-generated separate and combined auditory, visual, and somatosensory stimulation. These results were used to compare the multisensory features of neurons in cat primary auditory cortex (A1) with those identified in the nearby higher-order auditory region, the Dorsal Zone (DZ). Both regions exhibited the same forms of multisensory neurons, albeit in different proportions. Multisensory neurons exhibiting excitatory or inhibitory properties occurred in similar proportions in both areas. Also, multisensory neurons in both areas expressed similar levels of multisensory integration. Because responses to auditory cues alone were so similar to those that included non-auditory stimuli, it is proposed that this effect represents a mechanism by which multisensory neurons subserve the process of perceptual binding.
... Effects of cortical cooling in awake animals with our custom build probe was tested by investigating spiking properties recorded directly underneath the cooling probe ( Figure 5) advancing a single tungsten electrode through the recording hole (see Figure 1B). Based on the available literature Malhotra et al., 2004;Nakamoto et al., 2008;Coomber et al., 2011;Wood et al., 2017), we expected single units in the auditory cortex to display a reduction in both, spontaneous and stimulus driven spiking activity upon cooling. For the neuron shown in Figure 5A, recorded at a depth of 1.36 mm underneath the cooling probe, this was indeed observed. ...
... Effects of cortical cooling in awake animals with our custom build probe was tested by investigating spiking properties recorded directly underneath the cooling probe ( Figure 5) advancing a single tungsten electrode through the recording hole (see Figure 1B). Based on the available literature Malhotra et al., 2004;Nakamoto et al., 2008;Coomber et al., 2011;Wood et al., 2017), we expected single units in the auditory cortex to display a reduction in both, spontaneous and stimulus driven spiking activity upon cooling. For the neuron shown in Figure 5A, recorded at a depth of 1.36 mm underneath the cooling probe, this was indeed observed. ...
The auditory thalamus is the central nexus of bottom-up connections from the inferior colliculus and top-down connections from auditory cortical areas. While considerable efforts have been made to investigate feedforward processing of sounds in the auditory thalamus (medial geniculate body, MGB) of non-human primates, little is known about the role of corticofugal feedback in the MGB of awake non-human primates. Therefore, we developed a small, repositionable cooling probe to manipulate corticofugal feedback and studied neural responses in both auditory cortex and thalamus to sounds under conditions of normal and reduced cortical temperature. Cooling-induced increases in the width of extracellularly recorded spikes in auditory cortex were observed over the distance of several hundred micrometers away from the cooling probe. Cortical neurons displayed reduction in both spontaneous and stimulus driven firing rates with decreased cortical temperatures. In thalamus, cortical cooling led to increased spontaneous firing and either increased or decreased stimulus driven activity. Furthermore, response tuning to modulation frequencies of temporally modulated sounds and spatial tuning to sound source location could be altered (increased or decreased) by cortical cooling. Specifically, best modulation frequencies of individual MGB neurons could shift either toward higher or lower frequencies based on the vector strength or the firing rate. The tuning of MGB neurons for spatial location could both sharpen or widen. Elevation preference could shift toward higher or lower elevations and azimuth tuning could move toward ipsilateral or contralateral locations. Such bidirectional changes were observed in many parameters which suggests that the auditory thalamus acts as a filter that could be adjusted according to behaviorally driven signals from auditory cortex. Future work will have to delineate the circuit elements responsible for the observed effects.
... A head holder was attached to the frontal bone of the skull using bone screws and dental acrylic. The animal was then provided with standard post-operative care (see Malhotra et al., 2004). In all cases, recovery was uneventful. ...
A basic function of the cerebral cortex is to receive and integrate information from different sensory modalities into a comprehensive percept of the environment. Neurons that demonstrate multisensory convergence occur across the necortex, but are especially prevalent in higher-order, association areas. However, a recent study of a cat higher-order auditory area, the dorsal zone (DZ) of auditory cortex, did not observe any multisensory features. Therefore, the goal of the present investigation was to address this conflict using recording and testing methodologies that are established for exposing and studying multisensory neuronal processing. Among the 482 neurons studied, we found that 76.6% were influenced by non-auditory stimuli. Of these neurons, 99% were affected by visual stimulation, but only 11% by somatosensory. Furthermore, a large proportion of the multisensory neurons showed integrated responses to multisensory stimulation, constituted a majority of the excitatory and inhibitory neurons encountered (as identified by the duration of their waveshape), and exhibited a distinct spatial distribution within DZ. These findings demonstrate that the dorsal zone of auditory cortex robustly exhibits multisensory properties and that the proportions of multisensory neurons encountered are consistent with those identified in other higher-order cortices.
... D'autre part, les lésions du cortex auditif entraînent des déficits dans les capacités de la localisation d'une source sonore chez l'animal (Kavanagh and Kelly, 1987 ;Malhotra, Hall and Lomber, 2004) et chez l'Homme (Klingon and Bontecou, 1966 ;Zatorre and Penhune, 2001) . ...
Introduction La surdité unilatérale est une pathologie fréquente chez l'enfant. Les répercussions en sont importantes tant sur le plan de l'audition spatiale que sur l'aspect du développement psychosocial. À ce jour, très peu de données neurofonctionnelles ont été recueillies chez l'enfant. L'objectif de cette thèse est donc d'étudier, chez l'enfant, le lien entre l'atteinte auditive unilatérale et ses corrélats neuraux. Cet objectif repose sur deux études, lesquelles sont définies comme suit : 1) Procéder à l'identification des paramètres de stimulation optimaux utilisés en fNIRS afin d'obtenir un signal de qualité sur l'enfant et, 2) Mesurer la réorganisation corticale suite à la surdité unilatérale et corréler cette réorganisation aux performances psychoacoustiques, psychosociales. Matériels et méthodes S'agissant de la première étude, dix-sept sujets adultes normo-entendants ont été recrutés. Ils ont été soumis à quatre conditions de stimulation auditive en fNIRS. L'amplitude du signal fNIRS enregistré et la durée expérimentale ont été comparées, entre ces conditions. Concernant la seconde étude, quatre enfants porteurs de surdité unilatérale ont été inclus. Ils ont été évalués en psychoacoustique par les tests de localisation du son dans l'espace et de la compréhension de la parole dans le bruit, en neurofonctionnel par la fNIRS, et en développement psychosocial par les tests mesurant les habiletés linguistiques différentes. Ils ont enfin répondu aux questionnaires de qualité de vie. Résultats L'étude 1 a identifié la durée de stimulation de 15 s comme étant un choix optimal, lorsqu'elle est associée à une amplitude trois fois plus importante et à une durée plus courte de 105 s que les autres conditions de stimulation. L'étude 2 a démontré une grande variabilité des résultats en performances psychoacoustiques et psychosociales. De plus, la surdité unilatérale a induit une augmentation de l'activation corticale ipsilatérale à l'oreille saine. Cette augmentation est significativement corrélée aux performances binaurales. Conclusion La surdité unilatérale induit des phénomènes de réorganisation corticale associés à une forte variabilité des performances binaurales et psychosociales, suggérant l'existence de facteurs compensatoires. Ce travail souligne la nécessité de l'identification de ces facteurs compensatoires et d'une prise en charge des enfants vulnérables aux effets néfastes de la surdité unilatérale.
... In hearing, location in space is a prominent attribute of a sound source, and it seems reasonable to search for point-to-point maps of the locations of sound sources in the world onto locations in the auditory cortex. In support of that quest are observations that unilateral lesions or inactivation of auditory cortex can disrupt performance of operant tasks requiring localization of contralateral sounds (Jenkins and Merzenich, 1984;Malhotra et al., 2004), which demonstrate the necessity of cortical function for spatial hearing. Also, auditory space maps are found in subcortical structures (Knudsen and Konishi, 1978;Middlebrooks and Knudsen, 1984), which demonstrates the feasibility of topographic spatial representation in the brain. ...
... In my present understanding, a two-or three-channel representation of sound-source location greatly devalues the wealth of information that is carried by the varied spatial tuning of single neurons. Another limitation of such fewchannel representations is that they rely on the balance of activity between a large population of contralaterally tuned neurons and a much smaller population of ipsilaterally tuned neurons within each cortical hemisphere; comparisons between cortical hemispheres cannot account for the observation that unilateral cortical inactivation results in only a contralateral localization deficit (Malhotra et al., 2004). Also, opponent models produce high acuity for near-midline sounds, but markedly degraded acuity for lateral locations, much more so than is observed psychophysically (e.g., Makous and Middlebrooks, 1990). ...
... We compared the effects of task engagement on spatial sensitivity among neurons in area A1, the dorsal zone (DZ), and the posterior auditory field (PAF) (Lee and Middlebrooks, 2013), all of which are necessary for normal localization behavior (Malhotra et al., 2004(Malhotra et al., , 2008. Approximately 30% of neurons in DZ and PAF showed a long-latency response that was more location-sensitive than the onset response. ...
This is the story of a search for a cortical map of auditory space. The search began with a study that was reported in the first issue of the Journal of Neuroscience (Middlebrooks and Pettigrew, 1981, 1:107-120.). That paper described some unexpected features of spatial sensitivity in the auditory cortex while failing to demonstrate the expected map. In the ensuing 40 years, we have encountered: panoramic spatial coding by single neurons; a rich variety of response patterns that are unmasked in the absence of general anesthesia; sharpening of spatial sensitivity when an animal is engaged in a listening task; and reorganization of spatial sensitivity in the presence of competing sounds. We have not encountered a map, but not through lack of trying. On the basis of years of negative results by our group and others, and positive results that are inconsistent with static point-to-point topography, we are confident in concluding that there just ain't no map. Instead, we have come to appreciate the highly dynamic spatial properties of cortical neurons, which serve the needs of listeners in a changing sonic environment.
