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Functional MRI of auditory responses in the zebra finch forebrain reveals a hierarchical organisation based on signal strength but not selectivity.

Boumans T, Gobes SM, Poirier C, Theunissen FE, Vandersmissen L, Pintjens W, Verhoye M, Bolhuis JJ, Van der Linden A - PLoS ONE (2008)

Bottom Line: Zebra finch males were exposed to conspecific song, BOS and to synthetic variations on BOS that differed in spectro-temporal and/or modulation phase structure.In particular, we have shown that the overall signal strength to song and synthetic variations thereof was different within two sub-regions of Field L2: zone L2a was significantly more activated compared to the adjacent sub-region L2b.Based on our results we suggest that unlike nuclei in the song system, sub-regions in the primary auditory pallium do not show selectivity for the BOS, but appear to show different levels of activity with exposure to any sound according to their place in the auditory processing stream.

View Article: PubMed Central - PubMed

Affiliation: Bio-Imaging Lab, University of Antwerp, Antwerp, Belgium.

ABSTRACT

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.

Methods and findings: Using blood oxygen level-dependent (BOLD) fMRI, we investigated neural responsiveness to natural and manipulated self-generated vocalisations and compared the selectivity for BOS and conspecific song in different sub-regions of the thalamo-recipient area Field L. Zebra finch males were exposed to conspecific song, BOS and to synthetic variations on BOS that differed in spectro-temporal and/or modulation phase structure. We found significant differences in the strength of BOLD responses between regions L2a, L2b and CMM, but no inter-stimuli differences within regions. In particular, we have shown that the overall signal strength to song and synthetic variations thereof was different within two sub-regions of Field L2: zone L2a was significantly more activated compared to the adjacent sub-region L2b.

Conclusions: Based on our results we suggest that unlike nuclei in the song system, sub-regions in the primary auditory pallium do not show selectivity for the BOS, but appear to show different levels of activity with exposure to any sound according to their place in the auditory processing stream.

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Related in: MedlinePlus

Visualisation of Field L2 on high resolution T2-weighted SE images and regional analysis (see online edition for color figure).The figure displays how the subfields L2a and L2b in the study of Vates et al. [46] compare to the core of the darker ellipsoid region of our anatomical high resolution MR images that corresponds to the dense fibre track that defines sub-region L2. (Schematic illustration adapted from Vates et al. [46]; anatomical MR image from Poirier et al. [50]). By drawing lines rostral and caudal from L2, and a third perpendicular line, regional analysis could be performed in a caudal/ventral region that comprises L3 and NCM, a rostral/dorsal region that comprises CMM, a dorsal region that comprises L2b and a ventral region that comprises L2a. ABBREVIATIONS, Ch. O. = Optic Chiasm; CMM = caudal medial mesopallium; DLM = medial nucleus of the dorsolateral thalamus; FPL = lateral forebrain bundle; L2a, L2b, L3 = sub-regions of Field L; NCM = caudomedial nidopallium; Ov = nucleus ovoidalis; tOM = tractus occipitomesencephalicus; X = area X.
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pone-0003184-g003: Visualisation of Field L2 on high resolution T2-weighted SE images and regional analysis (see online edition for color figure).The figure displays how the subfields L2a and L2b in the study of Vates et al. [46] compare to the core of the darker ellipsoid region of our anatomical high resolution MR images that corresponds to the dense fibre track that defines sub-region L2. (Schematic illustration adapted from Vates et al. [46]; anatomical MR image from Poirier et al. [50]). By drawing lines rostral and caudal from L2, and a third perpendicular line, regional analysis could be performed in a caudal/ventral region that comprises L3 and NCM, a rostral/dorsal region that comprises CMM, a dorsal region that comprises L2b and a ventral region that comprises L2a. ABBREVIATIONS, Ch. O. = Optic Chiasm; CMM = caudal medial mesopallium; DLM = medial nucleus of the dorsolateral thalamus; FPL = lateral forebrain bundle; L2a, L2b, L3 = sub-regions of Field L; NCM = caudomedial nidopallium; Ov = nucleus ovoidalis; tOM = tractus occipitomesencephalicus; X = area X.

Mentions: All further image processing was performed in Matlab with custom written software. Individual analyses were performed. The pre-processed time series for each pixel were first thresholded at a level determined by a histogram of signal strengths in order to separate signal in brain regions from the signal in non-brain regions. The time series for each pixel consisted of the 12 time points acquired during stimulation and averaged over all stimulation periods followed by the 24 time points acquired during rest and averaged over all rest periods in the block design (Figure 2). A difference time signal was calculated by subtracting the first half of the rest time curve from the stimulation time curve point by point. Then 12 average signal differences were estimated by summing these difference curves for one time point, two time points, and so forth until the entire difference signal was summed. Twelve statistical tests of significance at each pixel (one sample t-test) were then performed for each of these twelve average signal differences. The number of time points in the sum – between 1 and 12 – that gave the highest significance over all pixels was then used to calculate the signal strength for each pixel. This number was different for the five different birds (9, 11, 11, 11, 12). The rationale for this procedure is that the observed BOLD signal was characterized by both an increase during stimulation and a decrease during rest. Moreover, both the increase and decrease started (and often peaked) at the very first time point but then, after the first or second time point, decreased monotonically to baseline, often before the end of the twelve images. Our simple procedure was designed in order to maximally detect this characteristic signal without adding the noise found at the end of the time trace. The reported signal strength for a significant pixel is then the best average signal difference divided by the global average signal difference that was obtained by averaging over all 12 time points in the sum. All non-significant pixels and all isolated statistically significant pixels were deleted from the analysis. Furthermore, we performed our analysis on a region of interest defined by the large contiguous region of activity centred around the primary auditory region. Figure 3 shows how we performed the analysis on distinct sub-regions. The darker band in the structural MR-image corresponds to the dense fibre track defining sub-region L2. By drawing lines at the rostral and caudal border of this band, and a third line perpendicular to these two lines near the center of the darker band, the activity was divided in a caudal region that comprises L3 and NCM, a rostral region that comprises CMM, and a ventral and dorsal region within Field L2 that comprises L2a and L2b, respectively.


Functional MRI of auditory responses in the zebra finch forebrain reveals a hierarchical organisation based on signal strength but not selectivity.

Boumans T, Gobes SM, Poirier C, Theunissen FE, Vandersmissen L, Pintjens W, Verhoye M, Bolhuis JJ, Van der Linden A - PLoS ONE (2008)

Visualisation of Field L2 on high resolution T2-weighted SE images and regional analysis (see online edition for color figure).The figure displays how the subfields L2a and L2b in the study of Vates et al. [46] compare to the core of the darker ellipsoid region of our anatomical high resolution MR images that corresponds to the dense fibre track that defines sub-region L2. (Schematic illustration adapted from Vates et al. [46]; anatomical MR image from Poirier et al. [50]). By drawing lines rostral and caudal from L2, and a third perpendicular line, regional analysis could be performed in a caudal/ventral region that comprises L3 and NCM, a rostral/dorsal region that comprises CMM, a dorsal region that comprises L2b and a ventral region that comprises L2a. ABBREVIATIONS, Ch. O. = Optic Chiasm; CMM = caudal medial mesopallium; DLM = medial nucleus of the dorsolateral thalamus; FPL = lateral forebrain bundle; L2a, L2b, L3 = sub-regions of Field L; NCM = caudomedial nidopallium; Ov = nucleus ovoidalis; tOM = tractus occipitomesencephalicus; X = area X.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2527133&req=5

pone-0003184-g003: Visualisation of Field L2 on high resolution T2-weighted SE images and regional analysis (see online edition for color figure).The figure displays how the subfields L2a and L2b in the study of Vates et al. [46] compare to the core of the darker ellipsoid region of our anatomical high resolution MR images that corresponds to the dense fibre track that defines sub-region L2. (Schematic illustration adapted from Vates et al. [46]; anatomical MR image from Poirier et al. [50]). By drawing lines rostral and caudal from L2, and a third perpendicular line, regional analysis could be performed in a caudal/ventral region that comprises L3 and NCM, a rostral/dorsal region that comprises CMM, a dorsal region that comprises L2b and a ventral region that comprises L2a. ABBREVIATIONS, Ch. O. = Optic Chiasm; CMM = caudal medial mesopallium; DLM = medial nucleus of the dorsolateral thalamus; FPL = lateral forebrain bundle; L2a, L2b, L3 = sub-regions of Field L; NCM = caudomedial nidopallium; Ov = nucleus ovoidalis; tOM = tractus occipitomesencephalicus; X = area X.
Mentions: All further image processing was performed in Matlab with custom written software. Individual analyses were performed. The pre-processed time series for each pixel were first thresholded at a level determined by a histogram of signal strengths in order to separate signal in brain regions from the signal in non-brain regions. The time series for each pixel consisted of the 12 time points acquired during stimulation and averaged over all stimulation periods followed by the 24 time points acquired during rest and averaged over all rest periods in the block design (Figure 2). A difference time signal was calculated by subtracting the first half of the rest time curve from the stimulation time curve point by point. Then 12 average signal differences were estimated by summing these difference curves for one time point, two time points, and so forth until the entire difference signal was summed. Twelve statistical tests of significance at each pixel (one sample t-test) were then performed for each of these twelve average signal differences. The number of time points in the sum – between 1 and 12 – that gave the highest significance over all pixels was then used to calculate the signal strength for each pixel. This number was different for the five different birds (9, 11, 11, 11, 12). The rationale for this procedure is that the observed BOLD signal was characterized by both an increase during stimulation and a decrease during rest. Moreover, both the increase and decrease started (and often peaked) at the very first time point but then, after the first or second time point, decreased monotonically to baseline, often before the end of the twelve images. Our simple procedure was designed in order to maximally detect this characteristic signal without adding the noise found at the end of the time trace. The reported signal strength for a significant pixel is then the best average signal difference divided by the global average signal difference that was obtained by averaging over all 12 time points in the sum. All non-significant pixels and all isolated statistically significant pixels were deleted from the analysis. Furthermore, we performed our analysis on a region of interest defined by the large contiguous region of activity centred around the primary auditory region. Figure 3 shows how we performed the analysis on distinct sub-regions. The darker band in the structural MR-image corresponds to the dense fibre track defining sub-region L2. By drawing lines at the rostral and caudal border of this band, and a third line perpendicular to these two lines near the center of the darker band, the activity was divided in a caudal region that comprises L3 and NCM, a rostral region that comprises CMM, and a ventral and dorsal region within Field L2 that comprises L2a and L2b, respectively.

Bottom Line: Zebra finch males were exposed to conspecific song, BOS and to synthetic variations on BOS that differed in spectro-temporal and/or modulation phase structure.In particular, we have shown that the overall signal strength to song and synthetic variations thereof was different within two sub-regions of Field L2: zone L2a was significantly more activated compared to the adjacent sub-region L2b.Based on our results we suggest that unlike nuclei in the song system, sub-regions in the primary auditory pallium do not show selectivity for the BOS, but appear to show different levels of activity with exposure to any sound according to their place in the auditory processing stream.

View Article: PubMed Central - PubMed

Affiliation: Bio-Imaging Lab, University of Antwerp, Antwerp, Belgium.

ABSTRACT

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.

Methods and findings: Using blood oxygen level-dependent (BOLD) fMRI, we investigated neural responsiveness to natural and manipulated self-generated vocalisations and compared the selectivity for BOS and conspecific song in different sub-regions of the thalamo-recipient area Field L. Zebra finch males were exposed to conspecific song, BOS and to synthetic variations on BOS that differed in spectro-temporal and/or modulation phase structure. We found significant differences in the strength of BOLD responses between regions L2a, L2b and CMM, but no inter-stimuli differences within regions. In particular, we have shown that the overall signal strength to song and synthetic variations thereof was different within two sub-regions of Field L2: zone L2a was significantly more activated compared to the adjacent sub-region L2b.

Conclusions: Based on our results we suggest that unlike nuclei in the song system, sub-regions in the primary auditory pallium do not show selectivity for the BOS, but appear to show different levels of activity with exposure to any sound according to their place in the auditory processing stream.

Show MeSH
Related in: MedlinePlus