Limits...
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.

Show MeSH

Related in: MedlinePlus

Reconstructed plots of recording sites of dopaminergic neurons showing excitatory or inhibitory initial response components. Colored circles indicate the location of dopaminergic neurons in the SNc showing excitatory (green) or inhibitory (red) initial components in response to cortical stimulation (either single pulses or pulse trains) at baseline. Recording positions are reconstructed onto coronal sections, the position of which is given relative to bregma. The SNc is indicated by shading.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3921396&req=5

Figure 7: Reconstructed plots of recording sites of dopaminergic neurons showing excitatory or inhibitory initial response components. Colored circles indicate the location of dopaminergic neurons in the SNc showing excitatory (green) or inhibitory (red) initial components in response to cortical stimulation (either single pulses or pulse trains) at baseline. Recording positions are reconstructed onto coronal sections, the position of which is given relative to bregma. The SNc is indicated by shading.

Mentions: After intracollicular bicuculline, the majority (22/24) of DA neurons exhibited a short-latency, phasic excitatory (14/22) or inhibitory (8/22) response to light flash stimuli (Fig. 3, A and C; cf. Dommett et al. 2005). Although there was no overall change in the baseline firing rate of DA neurons (Table 1), after bicuculline, 9/16 of the cells that were previously unresponsive to single-pulse cortical stimulation now showed a short-latency excitation (5/16) or inhibition (4/16; Fig. 3, B and D) following collicular disinhibition. Neurons that already responded in the absence of bicuculline reacted to the treatment by decreasing their response latency (n = 3/8; pre 50.0 ± 26.5 ms vs. post 21.7 ± 10.1 ms), becoming unresponsive (n = 2/8) or changing the sign of their responses (n = 3/8; see Fig. 6A). As a consequence of the ability to switch between response types, cells responding to cortical stimulation with either an initial excitation or an initial inhibition do not appear to constitute two separate populations of neurons (unlike DA neurons, which respond to noxious/aversive stimuli with excitations and inhibitions; Brischoux et al. 2009; Matsumoto and Hikosaka 2009; but see Fiorillo et al. 2013b). This conclusion is supported by the fact that those DA neurons that exhibited initial excitations to either single-pulse electrical stimulation (predrug) or pulse trains did not differ from those exhibiting initial inhibitions in terms of baseline activity (excited: 2.8 ± 0.6; inhibited: 3.1 ± 0.6; t[14.5] = 0.33, P > 0.05) or action potential shape (time from onset of the spike to the 1st trough, excited: 1.3 ± 0.1, inhibited: 1.4 ± 0.1; t[14.2] = 1.14, P > 0.05). Likewise, there was no evidence of a systematic bias in the location of excited and inhibited cells in the SNc (Fig. 7).


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 recording sites of dopaminergic neurons showing excitatory or inhibitory initial response components. Colored circles indicate the location of dopaminergic neurons in the SNc showing excitatory (green) or inhibitory (red) initial components in response to cortical stimulation (either single pulses or pulse trains) at baseline. Recording positions are reconstructed onto coronal sections, the position of which is given relative to bregma. The SNc is indicated by shading.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Reconstructed plots of recording sites of dopaminergic neurons showing excitatory or inhibitory initial response components. Colored circles indicate the location of dopaminergic neurons in the SNc showing excitatory (green) or inhibitory (red) initial components in response to cortical stimulation (either single pulses or pulse trains) at baseline. Recording positions are reconstructed onto coronal sections, the position of which is given relative to bregma. The SNc is indicated by shading.
Mentions: After intracollicular bicuculline, the majority (22/24) of DA neurons exhibited a short-latency, phasic excitatory (14/22) or inhibitory (8/22) response to light flash stimuli (Fig. 3, A and C; cf. Dommett et al. 2005). Although there was no overall change in the baseline firing rate of DA neurons (Table 1), after bicuculline, 9/16 of the cells that were previously unresponsive to single-pulse cortical stimulation now showed a short-latency excitation (5/16) or inhibition (4/16; Fig. 3, B and D) following collicular disinhibition. Neurons that already responded in the absence of bicuculline reacted to the treatment by decreasing their response latency (n = 3/8; pre 50.0 ± 26.5 ms vs. post 21.7 ± 10.1 ms), becoming unresponsive (n = 2/8) or changing the sign of their responses (n = 3/8; see Fig. 6A). As a consequence of the ability to switch between response types, cells responding to cortical stimulation with either an initial excitation or an initial inhibition do not appear to constitute two separate populations of neurons (unlike DA neurons, which respond to noxious/aversive stimuli with excitations and inhibitions; Brischoux et al. 2009; Matsumoto and Hikosaka 2009; but see Fiorillo et al. 2013b). This conclusion is supported by the fact that those DA neurons that exhibited initial excitations to either single-pulse electrical stimulation (predrug) or pulse trains did not differ from those exhibiting initial inhibitions in terms of baseline activity (excited: 2.8 ± 0.6; inhibited: 3.1 ± 0.6; t[14.5] = 0.33, P > 0.05) or action potential shape (time from onset of the spike to the 1st trough, excited: 1.3 ± 0.1, inhibited: 1.4 ± 0.1; t[14.2] = 1.14, P > 0.05). Likewise, there was no evidence of a systematic bias in the location of excited and inhibited cells in the SNc (Fig. 7).

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