Dynamics of visually guided auditory plasticity in the optic tectum of the barn owl

1995 ◽  
Vol 73 (2) ◽  
pp. 595-614 ◽  
Author(s):  
M. S. Brainard ◽  
E. I. Knudsen

1. In the optic tectum of normal barn owls, bimodal (auditory-visual) neurons are tuned to the values of interaural time difference (ITD) that are produced by sounds at the locations of their visual receptive fields (VRFs). The auditory tuning of tectal neurons is actively guided by visual experience during development: in the tectum of adult owls reared with an optically displaced visual field, neurons are tuned to abnormal values of ITD that are close to the values produced by sounds at the locations of their optically displaced VRFs. In this study we investigated the dynamics of this experience-dependent plasticity. 2. Owls were raised from shortly after eye-opening (14-22 days of age) with prismatic spectacles that displaced the visual field to the right or left. Starting at approximately 60 days of age, multiunit recordings were made to assess the tuning of tectal neurons to ITD presented via earphones. In the earliest recording sessions (ages 60-80 days), ITD tuning was often close to normal, even though the majority of the owls' previous experience was with an altered correspondence between ITD values and VRF locations. Subsequently, over a period of weeks, responses to the normal range of ITDs were gradually eliminated while responses to values of ITD corresponding with the optically displaced VRF were acquired. 3. At intermediate stages in this process, the ITD tuning at many sites became abnormally broad, so that responses were simultaneously present to both normal values of ITD and to values corresponding with the optically displaced VRF. At this stage the latencies and durations of newly acquired responses systematically exceeded the latencies and durations of the responses to normal values of ITD. 4. Dynamic changes in ITD tuning similar to those recorded in the optic tectum also occurred in the external nucleus of the inferior colliculus (ICX), which provides the major source of ascending auditory input to the tectum. 5. These results suggest the hypothesis that the neural selectivity for ITD in the barn owl's tectum is first established by vision-independent mechanisms and only subsequently calibrated by visual experience. This calibration involves both the elimination of responses to normal values of ITD and the visually guided acquisition of responses to novel values and can be accounted for by plasticity at the level of the ICX.

1990 ◽  
Vol 64 (4) ◽  
pp. 1352-1360 ◽  
Author(s):  
M. R. Isley ◽  
D. C. Rogers-Ramachandran ◽  
P. G. Shinkman

1. The present experiments were designed to assess the effects of relatively large optically induced interocular torsional disparities on the developing kitten visual cortex. Kittens were reared with restricted visual experience. Three groups viewed a normal visual environment through goggles fitted with small prisms that introduced torsional disparities between the left and right eyes' visual fields, equal but opposite in the two eyes. Kittens in the +32 degrees goggle rearing condition experienced a 16 degrees counterclockwise rotation of the left visual field and a 16 degrees clockwise rotation of the right visual field; in the -32 degrees goggle condition the rotations were clockwise in the left eye and counterclockwise in the right. In the control (0 degree) goggle condition, the prisms did not rotate the visual fields. Three additional groups viewed high-contrast square-wave gratings through Polaroid filters arranged to provide a constant 32 degrees of interocular orientation disparity. 2. Recordings were made from neurons in visual cortex around the border of areas 17 and 18 in all kittens. Development of cortical ocular dominance columns was severely disrupted in all the experimental (rotated) rearing conditions. Most cells were classified in the extreme ocular dominance categories 1, 2, 6, and 7. Development of the system of orientation columns was also affected: among the relatively few cells with oriented receptive fields in both eyes, the distributions of interocular disparities in preferred stimulus orientation were centered near 0 degree but showed significantly larger variances than in the control condition.(ABSTRACT TRUNCATED AT 250 WORDS)


1994 ◽  
Vol 71 (1) ◽  
pp. 79-94 ◽  
Author(s):  
E. I. Knudsen ◽  
S. D. Esterly ◽  
J. F. Olsen

1. This study demonstrates the influence of experience on the establishment and maintenance of the auditory map of space in the optic tectum of the barn owl. Auditory experience was altered either by preventing the structures of the external ears (the facial ruff and preaural flaps) from appearing in baby barn owls (baby ruff-cut owls) or by removing these structures in adults (adult ruff-cut owls). These structures shape the binaural cues used for localizing sounds in both the horizontal and vertical dimensions. 2. The acoustic effects of removing the external ear structures were measured using probe tube microphones placed in the ear canals. In both baby and adult ruff-cut owls, the spatial pattern of binaural localization cues was dramatically different from normal: interaural level difference (ILD) changed with azimuth instead of with elevation, the rate of change of ILD across space was decreased relative to normal, and the rate of change of interaural time difference (ITD) across frontal space was increased relative to normal. 3. The neurophysiological representations of ITD and ILD in the optic tectum were measured before and > or = 3 mo after ruff removal in adults and beginning at 4.5 months of age in baby ruff-cut owls. Multiunit tuning to ITD and to ILD was measured using dichotic stimulation in ketamine-anesthetized owls. The tectal maps of ITD and ILD were reconstructed using visual receptive field location as a marker for recording site location in the optic tectum. 4. Adjustment of the tectal map of ITD to the altered spatial pattern of acoustic ITD was essentially complete in adults as well as in baby ruff-cut owls. This adjustment changed the magnification of ITD across the tectum, with resultant changes in ITD tuning at individual tectal sites of up to approximately 25 microseconds (approximately 5% of the physiological range) relative to normal values. 5. Adaptation of the tectal ILD map to the ruff-cut spatial pattern of acoustic ILD was substantial but clearly incomplete in both adult and baby ruff-cut owls. Although changes of up to approximately 15 dB (approximately 47% of the physiological range) relative to normal tuning were observed at certain tectal sites, the topography of the ILD map was always intermediate between normal and that predicted by the ruff-cut spatial pattern of acoustic ILD.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 11 (2) ◽  
pp. 153-166 ◽  
Author(s):  
Marie T. Banich ◽  
Kara D. Federmeier

In this study we examined Kosslyn's (1987) claim that the right hemisphere exhibits a relative superiority for processing metric spatial relations, whereas the left hemisphere exhibits a relative superiority for processing categorical spatial relations. In particular, we examined whether some failures to observe strong visual field (VF) advantages in previous studies might be due to practice effects that allowed individuals to process tasks in alternative manners (e.g., to process a metric task using a categorical strategy). We used two versions of a task previously employed by Hellige and Michimata (1989) in which individuals judge the metric (distance) or categorical (above/below) spatial relations between a bar and a dot. In one version, the position of the bar was held static. In another, the bar's position varied. This manipulation prevented participants from using the computer screen as a reference frame, forcing them to compute the spatial relationships on the basis of the relevant items only (i.e., the bar and the dot). In the latter, but not the former version of the task we obtained evidence supporting Kosslyn's hypothesis, namely, a significant right visual field (RVF) advantage for categorical spatial processing and a trend toward a left visual field (LVF) advantage for metric spatial processing. Furthermore, the pattern of results for trials on which information was presented centrally (CVF trials) was similar to that observed on RVF trials, whereas the pattern for trials in which identical information was presented in each visual field (BVF trials) was similar to that observed on LVF trials. Such a pattern is consistent with Kosslyn's suggestion that categorical processing is better suited for cells with small receptive fields and metric processing for cells with larger receptive fields.


2019 ◽  
Author(s):  
Kun Wang ◽  
Julian Hinz ◽  
Yue Zhang ◽  
Tod R. Thiele ◽  
Aristides B Arrenberg

AbstractNon-cortical visual areas in vertebrate brains extract different stimulus features, such as motion, object size and location, to support behavioural tasks. The optic tectum and pretectum, two primary visual areas, are thought to fulfil complementary biological functions in zebrafish to support prey capture and optomotor stabilisation behaviour. However, the adaptations of these brain areas to behaviourally relevant stimulus statistics are unknown. Here, we used calcium imaging to characterize the receptive fields of 1,926 motion-sensitive neurons in diencephalon and midbrain. We show that many caudal pretectal neurons have large receptive fields (RFs), whereas RFs of tectal neurons are smaller and mostly size-selective. RF centres of large-size RF neurons in the pretectum are predominantly located in the lower visual field, while tectal neurons sample the upper-nasal visual field more densely. This tectal visual field sampling matches the expected prey item locations, suggesting that the tectal magnification of the upper-nasal visual field might be an adaptation to hunting behaviour. Finally, we probed optomotor responsiveness and found that even relatively small stimuli drive optomotor swimming, if presented in the lower-temporal visual field, suggesting that the pretectum preferably samples information from this region on the ground to inform optomotor behaviour. Our characterization of the parallel processing channels for non-cortical motion feature extraction provides a basis for further investigation into the sensorimotor transformations of the zebrafish brain and its adaptations to habitat and lifestyle.


2018 ◽  
Vol 119 (5) ◽  
pp. 1947-1961 ◽  
Author(s):  
Abigail C. Gambrill ◽  
Regina L. Faulkner ◽  
Hollis T. Cline

The circuit controlling visually guided behavior in nonmammalian vertebrates, such as Xenopus tadpoles, includes retinal projections to the contralateral optic tectum, where visual information is processed, and tectal motor outputs projecting ipsilaterally to hindbrain and spinal cord. Tadpoles have an intertectal commissure whose function is unknown, but it might transfer information between the tectal lobes. Differences in visual experience between the two eyes have profound effects on the development and function of visual circuits in animals with binocular vision, but the effects on animals with fully crossed retinal projections are not clear. We tested the effect of monocular visual experience on the visuomotor circuit in Xenopus tadpoles. We show that cutting the intertectal commissure or providing visual experience to one eye (monocular visual experience) is sufficient to disrupt tectally mediated visual avoidance behavior. Monocular visual experience induces asymmetry in tectal circuit activity across the midline. Repeated exposure to monocular visual experience drives maturation of the stimulated retinotectal synapses, seen as increased AMPA-to-NMDA ratios, induces synaptic plasticity in intertectal synaptic connections, and induces bilaterally asymmetric changes in the tectal excitation-to-inhibition ratio (E/I). We show that unilateral expression of peptides that interfere with AMPA or GABAA receptor trafficking alters E/I in the transfected tectum and is sufficient to degrade visuomotor behavior. Our study demonstrates that monocular visual experience in animals with fully crossed visual systems produces asymmetric circuit function across the midline and degrades visuomotor behavior. The data further suggest that intertectal inputs are an integral component of a bilateral visuomotor circuit critical for behavior. NEW & NOTEWORTHY The developing optic tectum of Xenopus tadpoles represents a unique circuit in which laterally positioned eyes provide sensory input to a circuit that is transiently monocular, but which will be binocular in the animal’s adulthood. We challenge the idea that the two lobes of tadpole optic tectum function independently by testing the requirement of interhemispheric communication and demonstrate that unbalanced sensory input can induce structural and functional plasticity in the tectum sufficient to disrupt function.


2017 ◽  
Author(s):  
Jesse Gomez ◽  
Vaidehi Natu ◽  
Brianna Jeska ◽  
Michael Barnett ◽  
Kalanit Grill-Spector

ABSTRACTReceptive fields (RFs) processing information in restricted parts of the visual field are a key property of neurons in the visual system. However, how RFs develop in humans is unknown. Using fMRI and population receptive field (pRF) modeling in children and adults, we determined where and how pRFs develop across the ventral visual stream. We find that pRF properties in visual field maps, V1 through VO1, are adult-like by age 5. However, pRF properties in face- and word-selective regions develop into adulthood, increasing the foveal representation and the visual field coverage for faces in the right hemisphere and words in the left hemisphere. Eye-tracking indicates that pRF changes are related to changing fixation patterns on words and faces across development. These findings suggest a link between viewing behavior of faces and words and the differential development of pRFs across visual cortex, potentially due to competition on foveal coverage.


1999 ◽  
Vol 82 (5) ◽  
pp. 2197-2209 ◽  
Author(s):  
Joshua I. Gold ◽  
Eric I. Knudsen

Bimodal, auditory-visual neurons in the optic tectum of the barn owl are sharply tuned for sound source location. The auditory receptive fields (RFs) of these neurons are restricted in space primarily as a consequence of their tuning for interaural time differences and interaural level differences across broad ranges of frequencies. In this study, we examined the extent to which frequency-specific features of early auditory experience shape the auditory spatial tuning of these neurons. We manipulated auditory experience by implanting in one ear canal an acoustic filtering device that altered the timing and level of sound reaching the eardrum in a frequency-dependent fashion. We assessed the auditory spatial tuning at individual tectal sites in normal owls and in owls raised with the filtering device. At each site, we measured a family of auditory RFs using broadband sound and narrowband sounds with different center frequencies both with and without the device in place. In normal owls, the narrowband RFs for a given site all included a common region of space that corresponded with the broadband RF and aligned with the site's visual RF. Acute insertion of the filtering device in normal owls shifted the locations of the narrowband RFs away from the visual RF, the magnitude and direction of the shifts depending on the frequency of the stimulus. In contrast, in owls that were raised wearing the device, narrowband and broadband RFs were aligned with visual RFs so long as the device was in the ear but not after it was removed, indicating that auditory spatial tuning had been adaptively altered by experience with the device. The frequency tuning of tectal neurons in device-reared owls was also altered from normal. The results demonstrate that experience during development adaptively modifies the representation of auditory space in the barn owl's optic tectum in a frequency-dependent manner.


2011 ◽  
Vol 106 (5) ◽  
pp. 2285-2302 ◽  
Author(s):  
Wanhua Shen ◽  
Caroline R. McKeown ◽  
James A. Demas ◽  
Hollis T. Cline

The balance of inhibitory to excitatory (I/E) synaptic inputs is thought to control information processing and behavioral output of the central nervous system. We sought to test the effects of the decreased or increased I/E ratio on visual circuit function and visually guided behavior in Xenopus tadpoles. We selectively decreased inhibitory synaptic transmission in optic tectal neurons by knocking down the γ2 subunit of the GABAA receptors (GABAAR) using antisense morpholino oligonucleotides or by expressing a peptide corresponding to an intracellular loop of the γ2 subunit, called ICL, which interferes with anchoring GABAAR at synapses. Recordings of miniature inhibitory postsynaptic currents (mIPSCs) and miniature excitatory PSCs (mEPSCs) showed that these treatments decreased the frequency of mIPSCs compared with control tectal neurons without affecting mEPSC frequency, resulting in an ∼50% decrease in the ratio of I/E synaptic input. ICL expression and γ2-subunit knockdown also decreased the ratio of optic nerve-evoked synaptic I/E responses. We recorded visually evoked responses from optic tectal neurons, in which the synaptic I/E ratio was decreased. Decreasing the synaptic I/E ratio in tectal neurons increased the variance of first spike latency in response to full-field visual stimulation, increased recurrent activity in the tectal circuit, enlarged spatial receptive fields, and lengthened the temporal integration window. We used the benzodiazepine, diazepam (DZ), to increase inhibitory synaptic activity. DZ increased optic nerve-evoked inhibitory transmission but did not affect evoked excitatory currents, resulting in an increase in the I/E ratio of ∼30%. Increasing the I/E ratio with DZ decreased the variance of first spike latency, decreased spatial receptive field size, and lengthened temporal receptive fields. Sequential recordings of spikes and excitatory and inhibitory synaptic inputs to the same visual stimuli demonstrated that decreasing or increasing the I/E ratio disrupted input/output relations. We assessed the effect of an altered I/E ratio on a visually guided behavior that requires the optic tectum. Increasing and decreasing I/E in tectal neurons blocked the tectally mediated visual avoidance behavior. Because ICL expression, γ2-subunit knockdown, and DZ did not directly affect excitatory synaptic transmission, we interpret the results of our study as evidence that partially decreasing or increasing the ratio of I/E disrupts several measures of visual system information processing and visually guided behavior in an intact vertebrate.


2019 ◽  
Author(s):  
Ethan J. Duwell ◽  
Erica N. Woertz ◽  
Jedidiah Mathis ◽  
Joseph Carroll ◽  
Edgar A. DeYoe

ABSTRACTRetinotopic organization is a fundamental feature of visual cortex thought to play a vital role in encoding spatial information. One important aspect of normal retinotopy is the representation of the right and left hemifields in contralateral visual cortex. However, in human albinism, many temporal retinal afferents decussate pathologically at the optic chiasm resulting in partially superimposed representations of opposite hemifields in each hemisphere of visual cortex. Previous fMRI studies in human albinism suggest that the right and left hemifield representations are superimposed in a mirror-symmetric manner. This should produce imaging voxels which respond to two separate regions in visual space mirrored across the vertical meridian. However, it is not yet clear how retino-cortical miswiring in albinism manifests at the level of single voxel population receptive fields. Here we used fMRI retinotopic mapping in conjunction with population receptive field (pRF) modeling to fit both single and dual pRF models to the visual responses of voxels in visual areas V1-V3 of five subjects with albinism. We found that subjects with albinism (but not controls) have sizable clusters of voxels with dual pRFs consistently corresponding to, but not fully coextensive with regions of hemifield overlap. These dual pRFs were typically positioned at roughly mirror image locations across the vertical meridian but were uniquely clustered within the visual field for each subject. We also found that single pRFs are larger in albinism than controls, and that single pRF sizes in the central visual field were anti-correlated with subjects’ foveal cone densities. Finally, dual pRF and aberrant hemifield representation characteristics varied significantly across subjects with albinism suggesting more central heterogeneity than previously appreciated.


1990 ◽  
Vol 5 (3) ◽  
pp. 231-239 ◽  
Author(s):  
B. J. Frost ◽  
L. Z. Wise ◽  
B. Morgan ◽  
D. Bird

AbstractLike many diurnal raptors, the American kestrel or sparrow hawk, Falco sparverius, possesses two foveae in each eye. In this study, we used fundus photography and reversed ophthalmoscopy to plot the projection of these foveae onto the visual field, together with other retinal landmarks such as the pecten and ora terminali. From such data, it was determined that the central monocular fovea (CMF) and temporal binocular fovea (TBF) were separated by 36 deg and that the kestrel has 58 deg of binocular overlap when the eyes are appropriately converged. Single-cell and multi-unit recordings were used to systematically explore the tectal surface and map receptive fields (RF) onto a hemispheric screen. A retinotopic map of the tectal surface was produced from such data and revealed an expanded representation for each fovea on the tectum and a systematic increase in RF size from fovea to periphery. The functional significance of this organization is discussed.


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