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Cortical regulation of dopaminergic neurons: role of the midbrain superior colliculus.

Bertram C, Dahan L, Boorman LW, Harris S, Vautrelle N, Leriche M, Redgrave P, Overton PG - J. Neurophysiol. (2013)

Bottom Line: In the case of vision, an important source of short-latency sensory information seems to be the midbrain superior colliculus (SC).Although single pulses produced small phasic activations in the colliculus, they did not elicit responses in the majority of DA neurons.Taken together, the results indicate that the cortex can communicate with DA neurons via a relay in the SC.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Sheffield, Western Bank, Sheffield, United Kingdom; and.

ABSTRACT
Dopaminergic (DA) neurons respond to stimuli in a wide range of modalities, although the origin of the afferent sensory signals has only recently begun to emerge. In the case of vision, an important source of short-latency sensory information seems to be the midbrain superior colliculus (SC). However, longer-latency responses have been identified that are less compatible with the primitive perceptual capacities of the colliculus. Rather, they seem more in keeping with the processing capabilities of the cortex. Given that there are robust projections from the cortex to the SC, we examined whether cortical information could reach DA neurons via a relay in the colliculus. The somatosensory barrel cortex was stimulated electrically in the anesthetized rat with either single pulses or pulse trains. Although single pulses produced small phasic activations in the colliculus, they did not elicit responses in the majority of DA neurons. However, after disinhibitory intracollicular injections of the GABAA antagonist bicuculline, collicular responses were substantially enhanced and previously unresponsive DA neurons now exhibited phasic excitations or inhibitions. Pulse trains applied to the cortex led to phasic changes (excitations to inhibitions) in the activity of DA neurons at baseline. These were blocked or attenuated by intracollicular administration of the GABAA agonist muscimol. Taken together, the results indicate that the cortex can communicate with DA neurons via a relay in the SC. As a consequence, DA neuronal activity reflecting the unexpected occurrence of salient events and that signaling more complex stimulus properties may have a common origin.

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Reconstructed plots of stimulation, recording, and injection sites. A: plots of stimulation sites in the cerebral cortex. Colored circles indicate the position of the electrode tips in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). S1, primary somatosensory cortex; S1BF, primary somatosensory cortex, barrel field; S1DZ, primary somatosensory cortex, dysgranular region; S2, secondary somatosensory cortex. B: reconstructed plots of recording/injection sites in the superior colliculus. Colored circles indicate the position of the recording/injection sites in animals in which muscimol was injected into the colliculus (red) or bicuculline was injected into the colliculus (blue). The layers are labeled as follows: 1, zonal layer; 2, superficial gray layer; 3, optic layer; 4, intermediate gray layer; 5, intermediate white layer; 6, deep gray layer; 7, deep white layer. C: reconstructed plots of recording sites in the substantia nigra pars compacta (SNc). Colored circles indicate the position of the recording sites in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). The point marked with a star represents the location of 2 recorded dopaminergic neurons. The SNc is indicated by shading. m, Substantia nigra medial part; l, substantia nigra lateral part; SNr, substantia nigra pars reticulata. In A–C, electrode positions are reconstructed onto coronal sections, the position of which is given relative to bregma.
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Figure 2: Reconstructed plots of stimulation, recording, and injection sites. A: plots of stimulation sites in the cerebral cortex. Colored circles indicate the position of the electrode tips in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). S1, primary somatosensory cortex; S1BF, primary somatosensory cortex, barrel field; S1DZ, primary somatosensory cortex, dysgranular region; S2, secondary somatosensory cortex. B: reconstructed plots of recording/injection sites in the superior colliculus. Colored circles indicate the position of the recording/injection sites in animals in which muscimol was injected into the colliculus (red) or bicuculline was injected into the colliculus (blue). The layers are labeled as follows: 1, zonal layer; 2, superficial gray layer; 3, optic layer; 4, intermediate gray layer; 5, intermediate white layer; 6, deep gray layer; 7, deep white layer. C: reconstructed plots of recording sites in the substantia nigra pars compacta (SNc). Colored circles indicate the position of the recording sites in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). The point marked with a star represents the location of 2 recorded dopaminergic neurons. The SNc is indicated by shading. m, Substantia nigra medial part; l, substantia nigra lateral part; SNr, substantia nigra pars reticulata. In A–C, electrode positions are reconstructed onto coronal sections, the position of which is given relative to bregma.

Mentions: 2D-OIS was used to assess the extent of spread of activation induced by the electrical stimulation parameters used to stimulate the barrel cortex in the present study. Single-pulse electrical stimulation of the cortex produced a localized region of enhanced activity (Fig. 1, A and B), which peaked 2.2 ± 0.3 s after stimulus onset and decreased rapidly both temporally and spatially (Fig. 1, C and D), having a radius at its peak of ∼2.0 mm (Fig. 1D). The response produced by single-pulse stimulation had a smaller peak amplitude, but a similar extent of spread, than whisker pad stimulation (Fig. 1D). The hemodynamic response elicited by a train of pulses had an extent of spread similar to that elicited by single pulses but had a greater peak amplitude (Fig. 1D). All stimulating electrode tips in the present study were located in the gray matter of the barrel cortex (Fig. 2A), which occupies ∼4.3 mm × 4.0 mm medio-laterally and rostro-caudally in these dimensions (Paxinos and Watson 2004); hence activation is likely to have been largely confined to the barrel cortex in all animals. Significant inclusion of the underlying white matter is contraindicated by the absence of activation of adjacent areas of the cortex within the thinned window (Fig. 1A).


Cortical regulation of dopaminergic neurons: role of the midbrain superior colliculus.

Bertram C, Dahan L, Boorman LW, Harris S, Vautrelle N, Leriche M, Redgrave P, Overton PG - J. Neurophysiol. (2013)

Reconstructed plots of stimulation, recording, and injection sites. A: plots of stimulation sites in the cerebral cortex. Colored circles indicate the position of the electrode tips in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). S1, primary somatosensory cortex; S1BF, primary somatosensory cortex, barrel field; S1DZ, primary somatosensory cortex, dysgranular region; S2, secondary somatosensory cortex. B: reconstructed plots of recording/injection sites in the superior colliculus. Colored circles indicate the position of the recording/injection sites in animals in which muscimol was injected into the colliculus (red) or bicuculline was injected into the colliculus (blue). The layers are labeled as follows: 1, zonal layer; 2, superficial gray layer; 3, optic layer; 4, intermediate gray layer; 5, intermediate white layer; 6, deep gray layer; 7, deep white layer. C: reconstructed plots of recording sites in the substantia nigra pars compacta (SNc). Colored circles indicate the position of the recording sites in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). The point marked with a star represents the location of 2 recorded dopaminergic neurons. The SNc is indicated by shading. m, Substantia nigra medial part; l, substantia nigra lateral part; SNr, substantia nigra pars reticulata. In A–C, electrode positions are reconstructed onto coronal sections, the position of which is given relative to bregma.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3921396&req=5

Figure 2: Reconstructed plots of stimulation, recording, and injection sites. A: plots of stimulation sites in the cerebral cortex. Colored circles indicate the position of the electrode tips in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). S1, primary somatosensory cortex; S1BF, primary somatosensory cortex, barrel field; S1DZ, primary somatosensory cortex, dysgranular region; S2, secondary somatosensory cortex. B: reconstructed plots of recording/injection sites in the superior colliculus. Colored circles indicate the position of the recording/injection sites in animals in which muscimol was injected into the colliculus (red) or bicuculline was injected into the colliculus (blue). The layers are labeled as follows: 1, zonal layer; 2, superficial gray layer; 3, optic layer; 4, intermediate gray layer; 5, intermediate white layer; 6, deep gray layer; 7, deep white layer. C: reconstructed plots of recording sites in the substantia nigra pars compacta (SNc). Colored circles indicate the position of the recording sites in animals in which pulse trains were applied to the cortex (red) or single pulses were applied to the cortex (blue). The point marked with a star represents the location of 2 recorded dopaminergic neurons. The SNc is indicated by shading. m, Substantia nigra medial part; l, substantia nigra lateral part; SNr, substantia nigra pars reticulata. In A–C, electrode positions are reconstructed onto coronal sections, the position of which is given relative to bregma.
Mentions: 2D-OIS was used to assess the extent of spread of activation induced by the electrical stimulation parameters used to stimulate the barrel cortex in the present study. Single-pulse electrical stimulation of the cortex produced a localized region of enhanced activity (Fig. 1, A and B), which peaked 2.2 ± 0.3 s after stimulus onset and decreased rapidly both temporally and spatially (Fig. 1, C and D), having a radius at its peak of ∼2.0 mm (Fig. 1D). The response produced by single-pulse stimulation had a smaller peak amplitude, but a similar extent of spread, than whisker pad stimulation (Fig. 1D). The hemodynamic response elicited by a train of pulses had an extent of spread similar to that elicited by single pulses but had a greater peak amplitude (Fig. 1D). All stimulating electrode tips in the present study were located in the gray matter of the barrel cortex (Fig. 2A), which occupies ∼4.3 mm × 4.0 mm medio-laterally and rostro-caudally in these dimensions (Paxinos and Watson 2004); hence activation is likely to have been largely confined to the barrel cortex in all animals. Significant inclusion of the underlying white matter is contraindicated by the absence of activation of adjacent areas of the cortex within the thinned window (Fig. 1A).

Bottom Line: In the case of vision, an important source of short-latency sensory information seems to be the midbrain superior colliculus (SC).Although single pulses produced small phasic activations in the colliculus, they did not elicit responses in the majority of DA neurons.Taken together, the results indicate that the cortex can communicate with DA neurons via a relay in the SC.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Sheffield, Western Bank, Sheffield, United Kingdom; and.

ABSTRACT
Dopaminergic (DA) neurons respond to stimuli in a wide range of modalities, although the origin of the afferent sensory signals has only recently begun to emerge. In the case of vision, an important source of short-latency sensory information seems to be the midbrain superior colliculus (SC). However, longer-latency responses have been identified that are less compatible with the primitive perceptual capacities of the colliculus. Rather, they seem more in keeping with the processing capabilities of the cortex. Given that there are robust projections from the cortex to the SC, we examined whether cortical information could reach DA neurons via a relay in the colliculus. The somatosensory barrel cortex was stimulated electrically in the anesthetized rat with either single pulses or pulse trains. Although single pulses produced small phasic activations in the colliculus, they did not elicit responses in the majority of DA neurons. However, after disinhibitory intracollicular injections of the GABAA antagonist bicuculline, collicular responses were substantially enhanced and previously unresponsive DA neurons now exhibited phasic excitations or inhibitions. Pulse trains applied to the cortex led to phasic changes (excitations to inhibitions) in the activity of DA neurons at baseline. These were blocked or attenuated by intracollicular administration of the GABAA agonist muscimol. Taken together, the results indicate that the cortex can communicate with DA neurons via a relay in the SC. As a consequence, DA neuronal activity reflecting the unexpected occurrence of salient events and that signaling more complex stimulus properties may have a common origin.

Show MeSH
Related in: MedlinePlus