Functional Magnetic Resonance Imaging in Zebra Finch Discerns the Neural Substrate Involved in Segregation of Conspecific Song From Background Noise (original) (raw)
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Functional Magnetic Resonance Imaging (fMRI) with Auditory Stimulation in Songbirds
Journal of Visualized Experiments, 2013
The neurobiology of birdsong, as a model for human speech, is a pronounced area of research in behavioural neuroscience. Whereas electrophysiology and molecular approaches allow the investigation of either different stimuli on few neurons, or one stimulus in large parts of the brain, blood oxygenation level dependent (BOLD) functional Magnetic Resonance Imaging (fMRI) allows combining both advantages, i.e. compare the neural activation induced by different stimuli in the entire brain at once. fMRI in songbirds is challenging because of the small size of their brains and because their bones and especially their skull comprise numerous air cavities, inducing important susceptibility artefacts. Gradient-echo (GE) BOLD fMRI has been successfully applied to songbirds 1-5 (for a review, see 6 ). These studies focused on the primary and secondary auditory brain areas, which are regions free of susceptibility artefacts. However, because processes of interest may occur beyond these regions, whole brain BOLD fMRI is required using an MRI sequence less susceptible to these artefacts. This can be achieved by using spin-echo (SE) BOLD fMRI . In this article, we describe how to use this technique in zebra finches (Taeniopygia guttata), which are small songbirds with a bodyweight of 15-25 g extensively studied in behavioural neurosciences of birdsong. The main topic of fMRI studies on songbirds is song perception and song learning. The auditory nature of the stimuli combined with the weak BOLD sensitivity of SE (compared to GE) based fMRI sequences makes the implementation of this technique very challenging.
Journal of Physiology-Paris, 2013
Songbirds provide an excellent model system exhibiting vocal learning associated with an extreme brain plasticity linked to quantifiable behavioral changes. This animal model has thus far been intensively studied using electrophysiological, histological and molecular mapping techniques. However, these approaches do not provide a global view of the brain and/or do not allow repeated measures, which are necessary to establish correlations between alterations in neural substrate and behavior. In contrast, functional Magnetic Resonance Imaging (fMRI) is a non-invasive in vivo technique which allows one (i) to study brain function in the same subject over time, and (ii) to address the entire brain at once. During the last decades, fMRI has become one of the most popular neuroimaging techniques in cognitive neuroscience for the study of brain activity during various tasks ranging from simple sensory-motor to highly cognitive tasks. By alternating various stimulation periods with resting periods during scanning, resting and task-specific regional brain activity can be determined with this technique. Despite its obvious benefits, fMRI has, until now, only been sparsely used to study cognition in non-human species such as songbirds. The Bio-Imaging Lab (University of Antwerp, Belgium) was the first to implement Blood Oxygen Level Dependent (BOLD) fMRI in songbirds -and in particular zebra finches -for the visualization of sound perception and processing in auditory and song control brain regions. The present article provides an overview of the establishment and optimization of this technique in our laboratory and of the resulting scientific findings. The introduction of fMRI in songbirds has opened new research avenues that permit experimental analysis of complex sensorimotor and cognitive processes underlying vocal communication in this animal model.
European Journal of Neuroscience, 2007
Song perception in songbirds, just as music and speech perception in humans, requires processing the spectral and temporal structure found in the succession of song-syllables. Using functional magnetic resonance imaging and synthetic songs that preserved exclusively either the temporal or the spectral structure of natural song, we investigated how vocalizations are processed in the avian forebrain. We found bilateral and equal activation of the primary auditory region, field L. The more ventral regions of field L showed depressed responses to the synthetic songs that lacked spectral structure. These ventral regions included subarea L3, medial-ventral subarea L and potentially the secondary auditory region caudal medial nidopallium. In addition, field L as a whole showed unexpected increased responses to the temporally filtered songs and this increase was the largest in the dorsal regions. These dorsal regions included L1 and the dorsal subareas L and L2b. Therefore, the ventral region of field L appears to be more sensitive to the preservation of both spectral and temporal information in the context of song processing. We did not find any differences in responses to playback of the bird's own song vs other familiar conspecific songs. We also investigated the effect of three commonly used anaesthetics on the blood oxygen level-dependent response: medetomidine, urethane and isoflurane. The extent of the area activated and the stimulus selectivity depended on the type of anaesthetic. We discuss these results in the context of what is known about the locus of action of the anaesthetics, and reports of neural activity measured in electrophysiological experiments.
PLOS One, 2008
Background: Male songbirds learn their songs from an adult tutor when they are young. A network of brain nuclei known as the 'song system' is the likely neural substrate for sensorimotor learning and production of song, but the neural networks involved in processing the auditory feedback signals necessary for song learning and maintenance remain unknown. Determining which regions show preferential responsiveness to the bird's own song (BOS) is of great importance because neurons sensitive to self-generated vocalisations could mediate this auditory feedback process. Neurons in the song nuclei and in a secondary auditory area, the caudal medial mesopallium (CMM), show selective responses to the BOS. The aim of the present study is to investigate the emergence of BOS selectivity within the network of primary auditory sub-regions in the avian pallium.
Neuroimage, 2005
Auditory fMRI in humans has recently received increasing attention from cognitive neuroscientists as a tool to understand mental processing of learned acoustic sequences and analyzing speech recognition and development of musical skills. The present study introduces this tool in a well-documented animal model for vocal learning, the songbird, and provides fundamental insight in the main technical issues associated with auditory fMRI in these songbirds. Stimulation protocols with various listening tasks lead to appropriate activation of successive relays in the songbirds' auditory pathway. The elicited BOLD response is also region and stimulus specific, and its temporal aspects provide accurate measures of the changes in brain physiology induced by the acoustic stimuli. Extensive repetition of an identical stimulus does not lead to habituation of the response in the primary or secondary telencephalic auditory regions of anesthetized subjects. The BOLD signal intensity changes during a stimulation and subsequent rest period have a very specific time course which shows a remarkable resemblance to auditory evoked BOLD responses commonly observed in human subjects. This observation indicates that auditory fMRI in the songbird may establish a link between auditory related neuro-imaging studies done in humans and the large body of neuro-ethological research on song learning and neuro-plasticity performed in songbirds. D
Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch
Journal of Neurobiology, 1993
Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to respond to sound stimuli. The auditory responses in one such nucleus, robustus archistriatalis (RA), were characterized by making multi-unit recordings in awake and anesthetized adult male zebra finches and in birds that had received lesions of the input to RA from the lateral part of the magnocellular nucleus of the anterior neostriatum (LMAN) or the Higher Vocal Center (HVC). In awake birds, RA neurons have a high level of spontaneous activity and vigorous auditory responses to song stimuli. Significantly greater responses are seen to the bird's own song (BOS) than to BOS played in reverse (REV) or to the songs of conspecifics (CON). Under ketamine-xylazine anesthesia, spontaneous activity is reduced, response latency increases and responses to BOS, REV and CON are indistinguishable. Responses obtained under urethane anesthesia are similar to those seen in awake birds. Thus, the pattern and selectivity of auditory responses in RA depend on the animal's state. Auditory responses in RA are qualitatively unchanged following lesion of the input to RA from LMAN, indicating that this pathway is not required for the sensory processing that underlies the preference for BOS on the vocal production pathway. Our results show that an input other than that from LMAN must be primarily responsible for auditory responses in RA. The direct projection from HVC is the most likely pathway by which song selective auditory information arrives in RA, since lesioning HVC abolished auditory responses in RA.
Functional changes between seasons in the male songbird auditory forebrain
Frontiers in behavioral neuroscience, 2013
Songbirds are an excellent model for investigating the perception of learned complex acoustic communication signals. Male European starlings (Sturnus vulgaris) sing throughout the year distinct types of song that bear either social or individual information. Although the relative importance of social and individual information changes seasonally, evidence of functional seasonal changes in neural response to these songs remains elusive. We thus decided to use in vivo functional magnetic resonance imaging (fMRI) to examine auditory responses of male starlings that were exposed to songs that convey different levels of information (species-specific and group identity or individual identity), both during (when mate recognition is particularly important) and outside the breeding season (when group recognition is particularly important). We report three main findings: (1) the auditory area caudomedial nidopallium (NCM), an auditory region that is analogous to the mammalian auditory cortex,...