Dopaminergic modulation of spiny neurons in the turtle striatum

Abstract

Intracellular recordings were obtained from brain slice preparation in neurons of the striatum of the turtle Trachemys scripta elegans, analogous to the mammalian striatum in its topographic organization, synaptic connectivity, cytoarchitecture, and neurochemistry. Here we show that these similarities extend to the electrophysiological properties of its neurons. Biocytin staining revealed that 85% of the recorded neurons were medium spiny neurons while 15% were aspiny neurons. Spiny neurons of the turtle resembled those found in the mammalian and avian striatum and express dopaminergic D(1) and D(2) class receptors. Because the striatum of the turtle receives a dense dopaminergic innervation from tegmental dopaminergic neurons we investigated the postsynaptic actions of selective dopamine receptor agonists in the excitability of spiny neurons. As in mammals and birds, activation of D(1)-receptors enhances, whereas activation of D(2)-receptors decreases the evoked discharge. Apparently, actions of dopamine agonists occur via the modulation of L-type (Ca(V)1) Ca2+-conductances. Strong cellular evidence suggests that the role of dopamine in the modulation of motor networks is preserved along vertebrate evolution.

Fig. 1

Medium spiny neurons of the striatum of the turtle. a Coronal sections through the turtle’s brain are shown schematically. Grey regions indicate the striatum (modified from Powers and Reiner, 1980) and dots show location and distribution of recorded neurons. b Camera lucida serial reconstruction of a recorded and biocytin-filled medium spiny neuron and c photomicrograph of the same neuron. d Top traces show injected depolarizing and hyperpolarizing current steps and bottom shows voltage responses to current pulse injections to the medium spiny neuron shown in b, c. Ramp-like increase in membrane potential and latency for first action potential firing (arrow) characterize these neurons. e Current–voltage relationship (I–V plot) measured from traces similar to those in d (empty circles) exhibits inward rectification. Line is a third-order polynomial fit to the data. Inset shows tonic-evoked discharge with frequency adaptation

Fig. 2

Activation of dopamine D₁-class receptors enhances the excitability of spiny neurons in the striatum of the turtle. a Control: repetitive discharge evoked by depolarizing rectangular current steps of increasing strength (at the bottom). b Evoked discharge after bath application of the selective dopamine D₁-receptor agonist SKF-81297 (1 μM). Firing frequency to the same current steps was increased. c Intensity–frequency relationships (I–F plots) built from traces as those in a–b. Note increased gain for similar stimuli after the D₁-agonist. d Paired line plot showing variation in mean frequency (measured at half maximum frequency in I–F plots) after addition of the D₁-agonist

Fig. 3

Activation of dopamine D₂-class receptors depresses the excitability of spiny neurons in the striatum of the turtle. a Control: repetitive discharge evoked by depolarizing rectangular current steps of increasing strength (at the bottom). b Evoked discharge after bath application of the selective dopamine D₂-receptor agonist quinelorane (1 μM). Firing frequency to the same current steps was decreased. c Intensity–frequency relationships (I–F plots) built from traces as those in a–b. Note decreased gain for similar stimuli after the D₂-agonist. d Paired line plot showing variation in mean frequency (measured at half maximum frequency in I–F plots) after addition of the D₂-agonist

Fig. 4

Subthreshold action of dopamine agonists in the striatum of the turtle. a As it is the case of mammalian striatal neurons (Hernández-López et al. 1997), spiny neurons in the striatum of the turtle may respond with prolonged subthreshold depolarizations (arrow at the control) to brief current stimulus (at the bottom) if given at a depolarized membrane potential (≈ −50 mV) (1). These depolarizations may last hundreds of milliseconds and may produce the firing of action potentials much time after the stimulus is over. In the turtle as in the rodent, dihydropyridines (5 μM nicardipine in this case) reduce the subthreshold response (2). Superimposed traces are shown in 3. b In neurons in which the subthreshold depolarization is not very prolonged (control in 1), bath applications of the dopaminergic D₁-class agonist SKF81297 (1 μM) (2) prolong the slow subthreshold response. 1 and 2 are superimposed in 3. c On the contrary, the dopaminergic D₂-class receptor agonist quinelorane (5 μM) reduces the duration of the subthreshold response and may abolish neuronal firing altogether (cf., 1 and 2)