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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.


Probabilistic tractography from IC in a common dolphin brain (Delphinus delphis). Using seeds drawn on the left (red) and right (blue) inferior colliculi (IC, upper left), a tract to the temporal lobe was identified, which passed through the ventrocaudal thalamus and the medial geniculate nucleus (MGN). The tract colour indicates the percentage of streamlines passing through a voxel and is thresholded such that voxels in which less than 20% of the streamlines pass are not shown. Insets show transverse slices at the level of the MGN (upper right) and cochlear nuclei (lower right) which shows the decussation of the auditory tract and entrance of the auditory nerves, and a sagittal slice through the left sylvian fissure (lower middle). Three-dimensional rendering (lower left) shows major landmarks. IC, inferior colliculus; sf, sylvian fissure; ss, suprasylvian sulcus; es, ectosylvian sulcus; cd, caudate; cbl, cerebellum.
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RSPB20151203F1: Probabilistic tractography from IC in a common dolphin brain (Delphinus delphis). Using seeds drawn on the left (red) and right (blue) inferior colliculi (IC, upper left), a tract to the temporal lobe was identified, which passed through the ventrocaudal thalamus and the medial geniculate nucleus (MGN). The tract colour indicates the percentage of streamlines passing through a voxel and is thresholded such that voxels in which less than 20% of the streamlines pass are not shown. Insets show transverse slices at the level of the MGN (upper right) and cochlear nuclei (lower right) which shows the decussation of the auditory tract and entrance of the auditory nerves, and a sagittal slice through the left sylvian fissure (lower middle). Three-dimensional rendering (lower left) shows major landmarks. IC, inferior colliculus; sf, sylvian fissure; ss, suprasylvian sulcus; es, ectosylvian sulcus; cd, caudate; cbl, cerebellum.

Mentions: With the IC seeds, we found a pathway to the ventrocaudal portion of the thalamus, which then turned laterally and terminated deep in the temporal lobe, near the sylvian fissure (figure 1). In the other direction, the fibres proceeded through the brainstem to the lateral lemniscus, superior olive and bilateral cochlear nuclei, confirming that we had identified the primary/ascending auditory pathway [23]. The tissue parameters of the second specimen (Stenella attenuata) indicated a shorter T1 of white matter (approx. 280 ms) than the Delphinus, suggesting more degradation had occurred in the Stenella with concomitant effects on the SNR of the diffusion images and a lower beff. Nevertheless, we confirmed the existence of these same pathways in the Stenella by seeding the IC and visualizing pathways to the MGN and temporal lobes, albeit at a lower threshold (electronic supplementary material, figure S1).FigureĀ 1.


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)

Probabilistic tractography from IC in a common dolphin brain (Delphinus delphis). Using seeds drawn on the left (red) and right (blue) inferior colliculi (IC, upper left), a tract to the temporal lobe was identified, which passed through the ventrocaudal thalamus and the medial geniculate nucleus (MGN). The tract colour indicates the percentage of streamlines passing through a voxel and is thresholded such that voxels in which less than 20% of the streamlines pass are not shown. Insets show transverse slices at the level of the MGN (upper right) and cochlear nuclei (lower right) which shows the decussation of the auditory tract and entrance of the auditory nerves, and a sagittal slice through the left sylvian fissure (lower middle). Three-dimensional rendering (lower left) shows major landmarks. IC, inferior colliculus; sf, sylvian fissure; ss, suprasylvian sulcus; es, ectosylvian sulcus; cd, caudate; cbl, cerebellum.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20151203F1: Probabilistic tractography from IC in a common dolphin brain (Delphinus delphis). Using seeds drawn on the left (red) and right (blue) inferior colliculi (IC, upper left), a tract to the temporal lobe was identified, which passed through the ventrocaudal thalamus and the medial geniculate nucleus (MGN). The tract colour indicates the percentage of streamlines passing through a voxel and is thresholded such that voxels in which less than 20% of the streamlines pass are not shown. Insets show transverse slices at the level of the MGN (upper right) and cochlear nuclei (lower right) which shows the decussation of the auditory tract and entrance of the auditory nerves, and a sagittal slice through the left sylvian fissure (lower middle). Three-dimensional rendering (lower left) shows major landmarks. IC, inferior colliculus; sf, sylvian fissure; ss, suprasylvian sulcus; es, ectosylvian sulcus; cd, caudate; cbl, cerebellum.
Mentions: With the IC seeds, we found a pathway to the ventrocaudal portion of the thalamus, which then turned laterally and terminated deep in the temporal lobe, near the sylvian fissure (figure 1). In the other direction, the fibres proceeded through the brainstem to the lateral lemniscus, superior olive and bilateral cochlear nuclei, confirming that we had identified the primary/ascending auditory pathway [23]. The tissue parameters of the second specimen (Stenella attenuata) indicated a shorter T1 of white matter (approx. 280 ms) than the Delphinus, suggesting more degradation had occurred in the Stenella with concomitant effects on the SNR of the diffusion images and a lower beff. Nevertheless, we confirmed the existence of these same pathways in the Stenella by seeding the IC and visualizing pathways to the MGN and temporal lobes, albeit at a lower threshold (electronic supplementary material, figure S1).FigureĀ 1.

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.