scholarly journals Auditory processing in the zebra finch midbrain: single unit responses and effect of rearing experience

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9363
Author(s):  
Priscilla Logerot ◽  
Paul F. Smith ◽  
Martin Wild ◽  
M. Fabiana Kubke

In birds the auditory system plays a key role in providing the sensory input used to discriminate between conspecific and heterospecific vocal signals. In those species that are known to learn their vocalizations, for example, songbirds, it is generally considered that this ability arises and is manifest in the forebrain, although there is no a priori reason why brainstem components of the auditory system could not also play an important part. To test this assumption, we used groups of normal reared and cross-fostered zebra finches that had previously been shown in behavioural experiments to reduce their preference for conspecific songs subsequent to cross fostering experience with Bengalese finches, a related species with a distinctly different song. The question we asked, therefore, is whether this experiential change also changes the bias in favour of conspecific song displayed by auditory midbrain units of normally raised zebra finches. By recording the responses of single units in MLd to a variety of zebra finch and Bengalese finch songs in both normally reared and cross-fostered zebra finches, we provide a positive answer to this question. That is, the difference in response to conspecific and heterospecific songs seen in normal reared zebra finches is reduced following cross-fostering. In birds the virtual absence of mammalian-like cortical projections upon auditory brainstem nuclei argues against the interpretation that MLd units change, as observed in the present experiments, as a result of top-down influences on sensory processing. Instead, it appears that MLd units can be influenced significantly by sensory inputs arising directly from a change in auditory experience during development.

1992 ◽  
Vol 336 (1278) ◽  
pp. 295-306 ◽  

The past 30 years has seen a remarkable development in our understanding of how the auditory system - particularly the peripheral system - processes complex sounds. Perhaps the most significant has been our understanding of the mechanisms underlying auditory frequency selectivity and their importance for normal and impaired auditory processing. Physiologically vulnerable cochlear filtering can account for many aspects of our normal and impaired psychophysical frequency selectivity with important consequences for the perception of complex sounds. For normal hearing, remarkable mechanisms in the organ of Corti, involving enhancement of mechanical tuning (in mammals probably by feedback of electro-mechanically generated energy from the hair cells), produce exquisite tuning, reflected in the tuning properties of cochlear nerve fibres. Recent comparisons of physiological (cochlear nerve) and psychophysical frequency selectivity in the same species indicate that the ear’s overall frequency selectivity can be accounted for by this cochlear filtering, at least in band width terms. Because this cochlear filtering is physiologically vulnerable, it deteriorates in deleterious conditions of the cochlea - hypoxia, disease, drugs, noise overexposure, mechanical disturbance - and is reflected in impaired psychophysical frequency selectivity. This is a fundamental feature of sensorineural hearing loss of cochlear origin, and is of diagnostic value. This cochlear filtering, particularly as reflected in the temporal patterns of cochlear fibres to complex sounds, is remarkably robust over a wide range of stimulus levels. Furthermore, cochlear filtering properties are a prime determinant of the ‘place’ and ‘time’ coding of frequency at the cochlear nerve level, both of which appear to be involved in pitch perception. The problem of how the place and time coding of complex sounds is effected over the ear’s remarkably wide dynamic range is briefly addressed. In the auditory brainstem, particularly the dorsal cochlear nucleus, are inhibitory mechanisms responsible for enhancing the spectral and temporal contrasts in complex sounds. These mechanisms are now being dissected neuropharmacologically. At the cortical level, mechanisms are evident that are capable of abstracting biologically relevant features of complex sounds. Fundamental studies of how the auditory system encodes and processes complex sounds are vital to promising recent applications in the diagnosis and rehabilitation of the hearing impaired.


2015 ◽  
Vol 32 (5) ◽  
pp. 445-459 ◽  
Author(s):  
Kyung Myun Lee ◽  
Erika Skoe ◽  
Nina Kraus ◽  
Richard Ashley

Acoustic periodicity is an important factor for discriminating consonant and dissonant intervals. While previous studies have found that the periodicity of musical intervals is temporally encoded by neural phase locking throughout the auditory system, how the nonlinearities of the auditory pathway influence the encoding of periodicity and how this effect is related to sensory consonance has been underexplored. By measuring human auditory brainstem responses (ABRs) to four diotically presented musical intervals with increasing degrees of dissonance, this study seeks to explicate how the subcortical auditory system transforms the neural representation of acoustic periodicity for consonant versus dissonant intervals. ABRs faithfully reflect neural activity in the brainstem synchronized to the stimulus while also capturing nonlinear aspects of auditory processing. Results show that for the most dissonant interval, which has a less periodic stimulus waveform than the most consonant interval, the aperiodicity of the stimulus is intensified in the subcortical response. The decreased periodicity of dissonant intervals is related to a larger number of nonlinearities (i.e., distortion products) in the response spectrum. Our findings suggest that the auditory system transforms the periodicity of dissonant intervals resulting in consonant and dissonant intervals becoming more distinct in the neural code than if they were to be processed by a linear auditory system.


2004 ◽  
Vol 91 (1) ◽  
pp. 136-151 ◽  
Author(s):  
Sarah M. N. Woolley ◽  
John H. Casseday

The avian mesencephalicus lateralis, dorsalis (MLd) is the auditory midbrain nucleus in which multiple parallel inputs from lower brain stem converge and through which most auditory information passes to reach the forebrain. Auditory processing in the MLd has not been investigated in songbirds. We studied the tuning properties of single MLd neurons in adult male zebra finches. Pure tones were used to examine tonotopy, temporal response patterns, frequency coding, intensity coding, spike latencies, and duration tuning. Most neurons had no spontaneous activity. The tonotopy of MLd is like that of other birds and mammals; characteristic frequencies (CFs) increase in a dorsal to ventral direction. Four major response patterns were found: 1) onset (49% of cells); 2) primary-like (20%); 3) sustained (19%); and 4) primary-like with notch (12%). CFs ranged between 0.9 and 6.1 kHz, matching the zebra finch hearing range and the power spectrum of song. Tuning curves were generally V-shaped, but complex curves, with multiple peaks or noncontiguous excitatory regions, were observed in 22% of cells. Rate-level functions indicated that 51% of nononset cells showed monotonic relationships between spike rate and sound level. Other cells showed low saturation or nonmonotonic responses. Spike latencies ranged from 4 to 40 ms, measured at CF. Spike latencies generally decreased with increasing sound pressure level (SPL), although paradoxical latency shifts were observed in 16% of units. For onset cells, changes in SPL produced smaller latency changes than for cells showing other response types. Results suggest that auditory midbrain neurons may be particularly suited for processing temporally complex signals with a high degree of precision.


Author(s):  
Leslie S. Smith

Audition is the ability to sense and interpret pressure waves within a range of frequencies. The system tries to solve the what and where tasks: what is the sound source (interpretation), and where is it (location)? Auditory environments vary in the number and location of sound sources, their level and in the degree of reverberation, yet biological systems have robust techniques that work over a large range of conditions. We briefly review the auditory system, including the auditory brainstem and mid-brain major components, attempting to connect its structure with the problems to be solved: locating some sounds, and interpreting important ones. Systems using knowledge of animal auditory processing are discussed, including both CPU-based and Neuromorphic approaches, starting from the auditory filterbank, and including silicon cochleae: feature (auditory landmark) based systems are considered. The level of performance associated with animal auditory systems has not been achieved, and we discuss ways forward.


2018 ◽  
Author(s):  
Allison L. Lansverk ◽  
Sarah E. London ◽  
Simon C. Griffith ◽  
David F. Clayton ◽  
Christopher N. Balakrishnan

ABSTRACTBirdsong is a classic example of a learned social behavior. Like many traits of interest, however, song production is also influenced by genetic factors and understanding the relative contributions of genetic and environmental influences remains a major research goal. In this study we take advantage of genetic variation among captive zebra finch populations to examine variation in a population-level song trait: song variability. We find that zebra finch populations differ in levels of song variability. Domesticated T. g. castanotis populations displayed higher song diversity than more recently wild-derived populations of both zebra finch subspecies T. g. castanotis and T. g. guttata, the Timor zebra finch. To determine whether these differences could have a genetic basis, we cross-fostered domesticated T. g. castanotis and Timor zebra finches to Bengalese finches Lonchura striata domestica. Following cross-fostering, domesticated T. g. castanotis maintained a higher level of song diversity than T. g. guttata. We suggest that the high song variability of domesticated zebra finches may be a consequence of reduced purifying selection acting on song traits. Intraspecific differences in the mechanisms underlying song variability therefore represent an untapped opportunity for probing the mechanisms of song learning and production.


Behaviour ◽  
1989 ◽  
Vol 109 (3-4) ◽  
pp. 163-174 ◽  
Author(s):  
N.S. Clayton

AbstractMale zebra finches, Taeniopygia guttata, which have been cross-fostered to Bengalesc finches, Lonchura striata, learn Bengalese finch song elements with as much accuracy as a male learning from his natural father. However, these elements are sung in phrases which are more nearly zebra finch length and lack the repetitiveness typical of the elements in a Bengalese finch phrase. Male Bengalese finches are also capable of learning song from a zebra finch foster-father. Males vary substantially but they tend to produce fewer, more widely spaced zebra finch elements in a Bengalese finch-length phrase. Both species show selective song learning and it is suggested that phrase length and the absence or presence of repeated elements might act as important cues for species-specific learning. Cross-fostered Bengalese finches seem to learn less than cross-fostered zebra finches: possible reasons for this are discussed.


2005 ◽  
Vol 94 (2) ◽  
pp. 1143-1157 ◽  
Author(s):  
Sarah M. N. Woolley ◽  
John H. Casseday

The avian auditory midbrain nucleus, the mesencephalicus lateralis, dorsalis (MLd), is the first auditory processing stage in which multiple parallel inputs converge, and it provides the input to the auditory thalamus. We studied the responses of single MLd neurons to four types of modulated sounds: 1) white noise; 2) band-limited noise; 3) frequency modulated (FM) sweeps, and 4) sinusoidally amplitude-modulated tones (SAM) in adult male zebra finches. Responses were compared with the responses of the same neurons to pure tones in terms of temporal response patterns, thresholds, characteristic frequencies, frequency tuning bandwidths, tuning sharpness, and spike rate/intensity relationships. Most neurons responded well to noise. More than one-half of the neurons responded selectively to particular portions of the noise, suggesting that, unlike forebrain neurons, many MLd neurons can encode specific acoustic components of highly modulated sounds such as noise. Selectivity for FM sweep direction was found in only 13% of cells that responded to sweeps. Those cells also showed asymmetric tuning curves, suggesting that asymmetric inhibition plays a role in FM directional selectivity. Responses to SAM showed that MLd neurons code temporal modulation rates using both spike rate and synchronization. Nearly all cells showed low-pass or band-pass filtering properties for SAM. Best modulation frequencies matched the temporal modulations in zebra finch song. Results suggest that auditory midbrain neurons are well suited for encoding a wide range of complex sounds with a high degree of temporal accuracy rather than selectively responding to only some sounds.


Author(s):  
Laura Hurley

The inferior colliculus (IC) receives prominent projections from centralized neuromodulatory systems. These systems include extra-auditory clusters of cholinergic, dopaminergic, noradrenergic, and serotonergic neurons. Although these modulatory sites are not explicitly part of the auditory system, they receive projections from primary auditory regions and are responsive to acoustic stimuli. This bidirectional influence suggests the existence of auditory-modulatory feedback loops. A characteristic of neuromodulatory centers is that they integrate inputs from anatomically widespread and functionally diverse sets of brain regions. This connectivity gives neuromodulatory systems the potential to import information into the auditory system on situational variables that accompany acoustic stimuli, such as context, internal state, or experience. Once released, neuromodulators functionally reconfigure auditory circuitry through a variety of receptors expressed by auditory neurons. In addition to shaping ascending auditory information, neuromodulation within the IC influences behaviors that arise subcortically, such as prepulse inhibition of the startle response. Neuromodulatory systems therefore provide a route for integrative behavioral information to access auditory processing from its earliest levels.


The Oxford Handbook of the Auditory Brainstem provides an in-depth reference to the organization and function of ascending and descending auditory pathways in the mammalian brainstem. Individual chapters are organized along the auditory pathway, beginning with the cochlea and ending with the auditory midbrain. Each chapter provides an introduction to the respective area and summarizes our current knowledge before discussing the disputes and challenges that the field currently faces.The handbook emphasizes the numerous forms of plasticity that are increasingly observed in many areas of the auditory brainstem. Several chapters focus on neuronal modulation of function and plasticity on the synaptic, neuronal, and circuit level, especially during development, aging, and following peripheral hearing loss. In addition, the book addresses the role of trauma-induced maladaptive plasticity with respect to its contribution in generating central hearing dysfunction, such as hyperacusis and tinnitus.The book is intended for students and postdoctoral fellows starting in the auditory field and for researchers of related fields who wish to get an authoritative and up-to-date summary of the current state of auditory brainstem research. For clinical practitioners in audiology, otolaryngology, and neurology, the book is a valuable resource of information about the neuronal mechanisms that are currently discussed as major candidates for the generation of central hearing dysfunction.


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