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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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Location of the recording and injection sites in representative animals. Left: a coronal section at high and low (inset) magnification, showing the superior colliculus processed with tyrosine hydroxylase (TH) and c-fos immunohistochemistry. The section shows fos-like immunolabeling (black dots) in the colliculus as a result of neural activity induced by an injection of bicuculline. An electrolytic lesion at the recording/injection site is indicated by an arrow. Right: coronal sections at high and low (insets) magnification, processed with TH immunohistochemistry (top) and cresyl violet (bottom). Top: TH immunolabeling (purple cells and processes) in the ventral midbrain and the electrode track and recording site (arrow) in the SNc. Bottom: the site can be seen again as a blue dot (indicated by an arrow). The position of all sections is given relative to bregma. Scale bars, 1 mm. SuSC, superficial layers of the SC (zonal layer, superficial gray layer, and optic layer); DpSC, deep layers of the SC (intermediate gray and intermediate white layers, deep gray/white layers); PAG, periaqueductal grey; VTA, ventral tegmental area; ml, media lemniscus; fr, fasciculus retroflexus.
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Figure 5: Location of the recording and injection sites in representative animals. Left: a coronal section at high and low (inset) magnification, showing the superior colliculus processed with tyrosine hydroxylase (TH) and c-fos immunohistochemistry. The section shows fos-like immunolabeling (black dots) in the colliculus as a result of neural activity induced by an injection of bicuculline. An electrolytic lesion at the recording/injection site is indicated by an arrow. Right: coronal sections at high and low (insets) magnification, processed with TH immunohistochemistry (top) and cresyl violet (bottom). Top: TH immunolabeling (purple cells and processes) in the ventral midbrain and the electrode track and recording site (arrow) in the SNc. Bottom: the site can be seen again as a blue dot (indicated by an arrow). The position of all sections is given relative to bregma. Scale bars, 1 mm. SuSC, superficial layers of the SC (zonal layer, superficial gray layer, and optic layer); DpSC, deep layers of the SC (intermediate gray and intermediate white layers, deep gray/white layers); PAG, periaqueductal grey; VTA, ventral tegmental area; ml, media lemniscus; fr, fasciculus retroflexus.

Mentions: Local injections of the GABAA receptor antagonist bicuculline into the deep layers of the SC (see Fig. 5 for a typical recording/injection site in the colliculus and Fig. 2B for reconstructed plots of all sites) produced widespread disinhibition within the colliculus, as evidenced by an increase in baseline firing rate (Tables 1 and 2) and extensive expression of c-fos product, a marker for neuronal activation (Herrera and Robertson 1996; see Fig. 5). After intracollicular bicuculline, collicular neurons exhibited a short-latency, phasic excitation in response to the light flash (Fig. 3, A and C; Table 2; cf. Coizet et al. 2009; Dommett et al. 2005). At the same time, there was a significant increase in the magnitude and duration of the phasic response to single-pulse stimulation of the cortex, although the onset latency of the response did not change (Fig. 3, B and D; Table 1). The onset latency of the response to light flash stimuli was significantly longer than that to cortical stimulation (Tables 1 and 2; W = 576, P < 0.05).


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)

Location of the recording and injection sites in representative animals. Left: a coronal section at high and low (inset) magnification, showing the superior colliculus processed with tyrosine hydroxylase (TH) and c-fos immunohistochemistry. The section shows fos-like immunolabeling (black dots) in the colliculus as a result of neural activity induced by an injection of bicuculline. An electrolytic lesion at the recording/injection site is indicated by an arrow. Right: coronal sections at high and low (insets) magnification, processed with TH immunohistochemistry (top) and cresyl violet (bottom). Top: TH immunolabeling (purple cells and processes) in the ventral midbrain and the electrode track and recording site (arrow) in the SNc. Bottom: the site can be seen again as a blue dot (indicated by an arrow). The position of all sections is given relative to bregma. Scale bars, 1 mm. SuSC, superficial layers of the SC (zonal layer, superficial gray layer, and optic layer); DpSC, deep layers of the SC (intermediate gray and intermediate white layers, deep gray/white layers); PAG, periaqueductal grey; VTA, ventral tegmental area; ml, media lemniscus; fr, fasciculus retroflexus.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 5: Location of the recording and injection sites in representative animals. Left: a coronal section at high and low (inset) magnification, showing the superior colliculus processed with tyrosine hydroxylase (TH) and c-fos immunohistochemistry. The section shows fos-like immunolabeling (black dots) in the colliculus as a result of neural activity induced by an injection of bicuculline. An electrolytic lesion at the recording/injection site is indicated by an arrow. Right: coronal sections at high and low (insets) magnification, processed with TH immunohistochemistry (top) and cresyl violet (bottom). Top: TH immunolabeling (purple cells and processes) in the ventral midbrain and the electrode track and recording site (arrow) in the SNc. Bottom: the site can be seen again as a blue dot (indicated by an arrow). The position of all sections is given relative to bregma. Scale bars, 1 mm. SuSC, superficial layers of the SC (zonal layer, superficial gray layer, and optic layer); DpSC, deep layers of the SC (intermediate gray and intermediate white layers, deep gray/white layers); PAG, periaqueductal grey; VTA, ventral tegmental area; ml, media lemniscus; fr, fasciculus retroflexus.
Mentions: Local injections of the GABAA receptor antagonist bicuculline into the deep layers of the SC (see Fig. 5 for a typical recording/injection site in the colliculus and Fig. 2B for reconstructed plots of all sites) produced widespread disinhibition within the colliculus, as evidenced by an increase in baseline firing rate (Tables 1 and 2) and extensive expression of c-fos product, a marker for neuronal activation (Herrera and Robertson 1996; see Fig. 5). After intracollicular bicuculline, collicular neurons exhibited a short-latency, phasic excitation in response to the light flash (Fig. 3, A and C; Table 2; cf. Coizet et al. 2009; Dommett et al. 2005). At the same time, there was a significant increase in the magnitude and duration of the phasic response to single-pulse stimulation of the cortex, although the onset latency of the response did not change (Fig. 3, B and D; Table 1). The onset latency of the response to light flash stimuli was significantly longer than that to cortical stimulation (Tables 1 and 2; W = 576, P < 0.05).

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