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Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe.

Berns GS, Cook PF, Foxley S, Jbabdi S, Miller KL, Marino L - Proc. Biol. Sci. (2015)

Bottom Line: A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of 'associative' regions in lateral and caudal directions.However, the precise location of the auditory cortex and its connections are still unknown.Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1.

View Article: PubMed Central - PubMed

Affiliation: Psychology Department, Emory University, Atlanta, GA, USA gberns@emory.edu.

ABSTRACT
The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of 'associative' regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin (Delphinus delphis) and a pantropical dolphin (Stenella attenuata) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.

No MeSH data available.


Thalamic parcellation of Delphinus delphis based on cortical regions. Three regions of interest were defined: (i) visual cortex (red); (ii) auditory cortex based on traditional boundaries in the suprasylvian gyrus (green) and (iii) auditory region temporal cortex based on IC tractography (blue). Seeds within the entire thalamus were traced to these regions and thresholded above 20 000 streamlines. Each row shows a set of slices that correspond to a single cursor location. The upper row is located posteriorly through the cortex while the lower row is located through thalamus. The thalamic parcellations to the three regions demonstrate that the temporal region is primarily connected to the ventrocaudal region, presumably near the medial geniculate nucleus. The visual and auditory regions overlap substantially in the thalamus and are located more dorsally and rostrally.
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RSPB20151203F2: Thalamic parcellation of Delphinus delphis based on cortical regions. Three regions of interest were defined: (i) visual cortex (red); (ii) auditory cortex based on traditional boundaries in the suprasylvian gyrus (green) and (iii) auditory region temporal cortex based on IC tractography (blue). Seeds within the entire thalamus were traced to these regions and thresholded above 20 000 streamlines. Each row shows a set of slices that correspond to a single cursor location. The upper row is located posteriorly through the cortex while the lower row is located through thalamus. The thalamic parcellations to the three regions demonstrate that the temporal region is primarily connected to the ventrocaudal region, presumably near the medial geniculate nucleus. The visual and auditory regions overlap substantially in the thalamus and are located more dorsally and rostrally.

Mentions: Thalamic parcellation confirmed earlier electrophysiological findings that portions of the thalamus were, indeed, connected to suprasylvian-A1 (figure 2, green). The suprasyvian-A1 thalamic connections were located dorsal and rostral to the regions connected to the temporal lobe, which were located ventrocaudally, near the presumed location of the MGN (figure 2, blue). The V1 thalamic connections (red) had extensive overlap with the suprasylvian-A1 connections. However, our new analysis also indicated pathways between the deep temporal lobe and suprasylvian-A1 regions bilaterally (figure 3).FigureĀ 2.


Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe.

Berns GS, Cook PF, Foxley S, Jbabdi S, Miller KL, Marino L - Proc. Biol. Sci. (2015)

Thalamic parcellation of Delphinus delphis based on cortical regions. Three regions of interest were defined: (i) visual cortex (red); (ii) auditory cortex based on traditional boundaries in the suprasylvian gyrus (green) and (iii) auditory region temporal cortex based on IC tractography (blue). Seeds within the entire thalamus were traced to these regions and thresholded above 20 000 streamlines. Each row shows a set of slices that correspond to a single cursor location. The upper row is located posteriorly through the cortex while the lower row is located through thalamus. The thalamic parcellations to the three regions demonstrate that the temporal region is primarily connected to the ventrocaudal region, presumably near the medial geniculate nucleus. The visual and auditory regions overlap substantially in the thalamus and are located more dorsally and rostrally.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4528565&req=5

RSPB20151203F2: Thalamic parcellation of Delphinus delphis based on cortical regions. Three regions of interest were defined: (i) visual cortex (red); (ii) auditory cortex based on traditional boundaries in the suprasylvian gyrus (green) and (iii) auditory region temporal cortex based on IC tractography (blue). Seeds within the entire thalamus were traced to these regions and thresholded above 20 000 streamlines. Each row shows a set of slices that correspond to a single cursor location. The upper row is located posteriorly through the cortex while the lower row is located through thalamus. The thalamic parcellations to the three regions demonstrate that the temporal region is primarily connected to the ventrocaudal region, presumably near the medial geniculate nucleus. The visual and auditory regions overlap substantially in the thalamus and are located more dorsally and rostrally.
Mentions: Thalamic parcellation confirmed earlier electrophysiological findings that portions of the thalamus were, indeed, connected to suprasylvian-A1 (figure 2, green). The suprasyvian-A1 thalamic connections were located dorsal and rostral to the regions connected to the temporal lobe, which were located ventrocaudally, near the presumed location of the MGN (figure 2, blue). The V1 thalamic connections (red) had extensive overlap with the suprasylvian-A1 connections. However, our new analysis also indicated pathways between the deep temporal lobe and suprasylvian-A1 regions bilaterally (figure 3).FigureĀ 2.

Bottom Line: A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of 'associative' regions in lateral and caudal directions.However, the precise location of the auditory cortex and its connections are still unknown.Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1.

View Article: PubMed Central - PubMed

Affiliation: Psychology Department, Emory University, Atlanta, GA, USA gberns@emory.edu.

ABSTRACT
The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of 'associative' regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin (Delphinus delphis) and a pantropical dolphin (Stenella attenuata) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.

No MeSH data available.