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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: 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.

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.


Related in: MedlinePlus

Basal ganglia parcellation based on cortical regions in Delphinus delphis. Five regions were defined in the orbital (‘frontal’) lobes from the longitudinal fissure (red) progressing laterally and ventrally (blue, green and yellow) to the ventral orbital lobe (pink). Seeds within the entire basal ganglia were traced to these regions and thresholded above 20 000 streamlines. Bottom row shows two coronal slices through different parts of the basal ganglia. The dorsal portions of the basal ganglia are connected to the dorsal portions of the cortex (red, blue and green), while the ventral basal ganglia are connected to the ventrolateral (yellow) and ventral orbital lobe (pink).
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RSPB20151203F4: Basal ganglia parcellation based on cortical regions in Delphinus delphis. Five regions were defined in the orbital (‘frontal’) lobes from the longitudinal fissure (red) progressing laterally and ventrally (blue, green and yellow) to the ventral orbital lobe (pink). Seeds within the entire basal ganglia were traced to these regions and thresholded above 20 000 streamlines. Bottom row shows two coronal slices through different parts of the basal ganglia. The dorsal portions of the basal ganglia are connected to the dorsal portions of the cortex (red, blue and green), while the ventral basal ganglia are connected to the ventrolateral (yellow) and ventral orbital lobe (pink).

Mentions: To confirm that the thalamic parcellation and temporal auditory pathway were not a spurious result of DTI or probabilistic tractography, we also performed a similar parcellation of the basal ganglia based on connections to the orbital lobes (figure 4). This technique has been used in humans, and a rostrocaudal gradient has been observed with the ventral portions of the striatum connected to the medial and orbital cortices, while the dorsal striatum is connected to the premotor and motor cortices [34]. We found the same rostrocaudal gradient in the dolphin brain. Notably, the most ventral parts of the orbital lobe were connected to the most ventral portions of the dolphin striatum, while the most dorsal portions of the orbital lobe—presumably the motor and premotor cortices—were connected to the dorsal striatum. This provides further evidence for the validity of the tractography methods used in this study and demonstrates that the cetacean orbital lobes are connected to the basal ganglia in a pattern similar to the connectivity of frontal lobes to basal ganglia in primates.Figure 4.


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)

Basal ganglia parcellation based on cortical regions in Delphinus delphis. Five regions were defined in the orbital (‘frontal’) lobes from the longitudinal fissure (red) progressing laterally and ventrally (blue, green and yellow) to the ventral orbital lobe (pink). Seeds within the entire basal ganglia were traced to these regions and thresholded above 20 000 streamlines. Bottom row shows two coronal slices through different parts of the basal ganglia. The dorsal portions of the basal ganglia are connected to the dorsal portions of the cortex (red, blue and green), while the ventral basal ganglia are connected to the ventrolateral (yellow) and ventral orbital lobe (pink).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20151203F4: Basal ganglia parcellation based on cortical regions in Delphinus delphis. Five regions were defined in the orbital (‘frontal’) lobes from the longitudinal fissure (red) progressing laterally and ventrally (blue, green and yellow) to the ventral orbital lobe (pink). Seeds within the entire basal ganglia were traced to these regions and thresholded above 20 000 streamlines. Bottom row shows two coronal slices through different parts of the basal ganglia. The dorsal portions of the basal ganglia are connected to the dorsal portions of the cortex (red, blue and green), while the ventral basal ganglia are connected to the ventrolateral (yellow) and ventral orbital lobe (pink).
Mentions: To confirm that the thalamic parcellation and temporal auditory pathway were not a spurious result of DTI or probabilistic tractography, we also performed a similar parcellation of the basal ganglia based on connections to the orbital lobes (figure 4). This technique has been used in humans, and a rostrocaudal gradient has been observed with the ventral portions of the striatum connected to the medial and orbital cortices, while the dorsal striatum is connected to the premotor and motor cortices [34]. We found the same rostrocaudal gradient in the dolphin brain. Notably, the most ventral parts of the orbital lobe were connected to the most ventral portions of the dolphin striatum, while the most dorsal portions of the orbital lobe—presumably the motor and premotor cortices—were connected to the dorsal striatum. This provides further evidence for the validity of the tractography methods used in this study and demonstrates that the cetacean orbital lobes are connected to the basal ganglia in a pattern similar to the connectivity of frontal lobes to basal ganglia in primates.Figure 4.

Bottom Line: 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.

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.


Related in: MedlinePlus