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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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Intracollicular muscimol administration suppressed collicular and dopaminergic responses to cortical stimulation. A: raster displays (top) and PSTHs (bottom) show that collicular neurons (SC) in this animal exhibited a short-latency excitatory response to pulse trains applied to the barrel cortex (CTX; 0.1 ms, 0.6 mA; vertical dotted line). Likewise, a simultaneously recorded DA neuron showed a short-latency excitatory response to the pulse trains. After a collicular microinjection of muscimol (CTX+MUS) the collicular response to cortical stimulation was attenuated, as was the response of the DA neuron. The PSTH for the DA neuron shows the 3-point smoothed change in firing rate from baseline (ΔHz). B: as well as excitations, pulse trains applied to the barrel cortex could induce short-latency inhibitions in DA neurons. In the example shown here, intracollicular muscimol eliminated the DA neuron's response to cortical stimulation. C: trains of electrical stimuli applied to the barrel cortex produced excitatory responses in the SC to each pulse in the train (black trace). Intracollicular administration of muscimol reduced baseline activity and depressed the responses to stimulation (red trace). D: raster display (top) and PSTH (bottom) of a representative case showing that electrical stimulation of the barrel cortex with pulse trains (5 pulses at 150 Hz, 0.1 ms each, 0.6 mA) produced temporally stable responses in DA neurons.
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Figure 4: Intracollicular muscimol administration suppressed collicular and dopaminergic responses to cortical stimulation. A: raster displays (top) and PSTHs (bottom) show that collicular neurons (SC) in this animal exhibited a short-latency excitatory response to pulse trains applied to the barrel cortex (CTX; 0.1 ms, 0.6 mA; vertical dotted line). Likewise, a simultaneously recorded DA neuron showed a short-latency excitatory response to the pulse trains. After a collicular microinjection of muscimol (CTX+MUS) the collicular response to cortical stimulation was attenuated, as was the response of the DA neuron. The PSTH for the DA neuron shows the 3-point smoothed change in firing rate from baseline (ΔHz). B: as well as excitations, pulse trains applied to the barrel cortex could induce short-latency inhibitions in DA neurons. In the example shown here, intracollicular muscimol eliminated the DA neuron's response to cortical stimulation. C: trains of electrical stimuli applied to the barrel cortex produced excitatory responses in the SC to each pulse in the train (black trace). Intracollicular administration of muscimol reduced baseline activity and depressed the responses to stimulation (red trace). D: raster display (top) and PSTH (bottom) of a representative case showing that electrical stimulation of the barrel cortex with pulse trains (5 pulses at 150 Hz, 0.1 ms each, 0.6 mA) produced temporally stable responses in DA neurons.

Mentions: As expected from our previous work (Coizet et al. 2009; Dommett et al. 2005), neurons in the SC deep layers (for brevity, we refer to all layers below the superficial layers as “deep” here and below) were unresponsive to whole field light flash stimuli in urethane-anesthetized animals (Fig. 3A). However, single-pulse electrical stimulation of the barrel cortex produced very short-latency, short-duration excitatory responses in the deep layers of the colliculus, with low temporal variability (Fig. 3B; Table 1). Pulse trains also produced very short-latency, temporally stable excitatory responses in the colliculus (Fig. 4, A–C; see Table 3), which had significantly longer durations than those following single-pulse stimulation (t[13.8] = 3.4, P < 0.05) but similar onset latencies (W = 131.5, P > 0.05; measured with respect to 1st stimulus in the train). The excitatory response to pulse trains consisted of discrete, progressively decrementing responses to each pulse in the train, and response size lessened across the train, such that the responses to earlier stimuli in the train were larger than those to later stimuli in the train (Fig. 4C; t[8] = 2.81, P < 0.05; assessed by measuring the activity in the 6.5 ms following the 2nd and last pulse in the train).


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)

Intracollicular muscimol administration suppressed collicular and dopaminergic responses to cortical stimulation. A: raster displays (top) and PSTHs (bottom) show that collicular neurons (SC) in this animal exhibited a short-latency excitatory response to pulse trains applied to the barrel cortex (CTX; 0.1 ms, 0.6 mA; vertical dotted line). Likewise, a simultaneously recorded DA neuron showed a short-latency excitatory response to the pulse trains. After a collicular microinjection of muscimol (CTX+MUS) the collicular response to cortical stimulation was attenuated, as was the response of the DA neuron. The PSTH for the DA neuron shows the 3-point smoothed change in firing rate from baseline (ΔHz). B: as well as excitations, pulse trains applied to the barrel cortex could induce short-latency inhibitions in DA neurons. In the example shown here, intracollicular muscimol eliminated the DA neuron's response to cortical stimulation. C: trains of electrical stimuli applied to the barrel cortex produced excitatory responses in the SC to each pulse in the train (black trace). Intracollicular administration of muscimol reduced baseline activity and depressed the responses to stimulation (red trace). D: raster display (top) and PSTH (bottom) of a representative case showing that electrical stimulation of the barrel cortex with pulse trains (5 pulses at 150 Hz, 0.1 ms each, 0.6 mA) produced temporally stable responses in DA neurons.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Intracollicular muscimol administration suppressed collicular and dopaminergic responses to cortical stimulation. A: raster displays (top) and PSTHs (bottom) show that collicular neurons (SC) in this animal exhibited a short-latency excitatory response to pulse trains applied to the barrel cortex (CTX; 0.1 ms, 0.6 mA; vertical dotted line). Likewise, a simultaneously recorded DA neuron showed a short-latency excitatory response to the pulse trains. After a collicular microinjection of muscimol (CTX+MUS) the collicular response to cortical stimulation was attenuated, as was the response of the DA neuron. The PSTH for the DA neuron shows the 3-point smoothed change in firing rate from baseline (ΔHz). B: as well as excitations, pulse trains applied to the barrel cortex could induce short-latency inhibitions in DA neurons. In the example shown here, intracollicular muscimol eliminated the DA neuron's response to cortical stimulation. C: trains of electrical stimuli applied to the barrel cortex produced excitatory responses in the SC to each pulse in the train (black trace). Intracollicular administration of muscimol reduced baseline activity and depressed the responses to stimulation (red trace). D: raster display (top) and PSTH (bottom) of a representative case showing that electrical stimulation of the barrel cortex with pulse trains (5 pulses at 150 Hz, 0.1 ms each, 0.6 mA) produced temporally stable responses in DA neurons.
Mentions: As expected from our previous work (Coizet et al. 2009; Dommett et al. 2005), neurons in the SC deep layers (for brevity, we refer to all layers below the superficial layers as “deep” here and below) were unresponsive to whole field light flash stimuli in urethane-anesthetized animals (Fig. 3A). However, single-pulse electrical stimulation of the barrel cortex produced very short-latency, short-duration excitatory responses in the deep layers of the colliculus, with low temporal variability (Fig. 3B; Table 1). Pulse trains also produced very short-latency, temporally stable excitatory responses in the colliculus (Fig. 4, A–C; see Table 3), which had significantly longer durations than those following single-pulse stimulation (t[13.8] = 3.4, P < 0.05) but similar onset latencies (W = 131.5, P > 0.05; measured with respect to 1st stimulus in the train). The excitatory response to pulse trains consisted of discrete, progressively decrementing responses to each pulse in the train, and response size lessened across the train, such that the responses to earlier stimuli in the train were larger than those to later stimuli in the train (Fig. 4C; t[8] = 2.81, P < 0.05; assessed by measuring the activity in the 6.5 ms following the 2nd and last pulse in the train).

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