Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics

Abstract

Transient, elevated concentrations of extracellular dopamine were characterized in the dorsal and ventral striatum of male rats during solitude, brief interaction with a conspecific, and copulation. Conspecific rats were systematically presented to male rats and allowed to interact for 30 sec; the males were kept in solitude between each presentation. During these episodes, 125 dopamine concentration transients from 17 rats were detected with fast-scan cyclic voltammetry at carbon-fiber microelectrodes (peak amplitude, 210 +/- 10 nm; duration, 530 +/- 20 msec). The frequency of dopamine transients increased sixfold during conspecific episodes compared with solitude. However, the phasic dopamine activity habituated on the second presentation of the conspecifics. When males were allowed to copulate with receptive females, additional dopamine transients were observed at frequencies approximately 20% of those during the previous interaction episodes. A subset of these transients immediately preceded intromission. Overall, phasic dopamine activity appeared to be associated with input from multiple sensory modalities and was followed by a variety of approach and appetitive behaviors, consistent with electrophysiological observations of dopaminergic neuron burst-firing. In summary, (1) dopamine concentration transients occur in awake rats during solitude, in the absence of overt external cues; (2) dopamine transients are significantly more frequent in the presence of a conspecific, although this effect habituates; and (3) dopamine transients are less frequent during copulation than during brief conspecific episodes. These results establish for the first time that transient dopamine fluctuations occur throughout the dorsal and ventral striatum and demonstrate that they are more frequent with salient stimuli that elicit a response behavior.

Fig. 1.

Representation of the carbon-fiber microelectrode recording sites in the dorsal and ventral striatum, as constructed from histological sections. The rectangles,circles, and triangles represent placements in the CP, NA, and OT, respectively.

Fig. 2.

Dopamine concentration transients in the CP, NA, and OT: solitude versus brief conspecific interaction.A, Frequency of transients by brain region and episode; *p < 0.0001; **p < 0.01, less frequent than NA and OT. B, Duration of transients by brain region and episode; *p < 0.0001.C, Peak concentration of transients by brain region and episode; *p < 0.01.

Fig. 3.

Histogram of dopamine concentration transients during the brief conspecific interaction episodes. Transients from all striatal regions and all interaction episodes were pooled into 2 sec bins, with the introduction of the conspecific at time 0. The presence of the conspecific is denoted by the gray bar from 0 to 30 sec.

Fig. 4.

Two dopamine concentration transients in the OT of a male rat associated with the introduction of a receptive female to the test chamber and subsequent contact. A, A 4 sec trace of the electrochemical signal at the oxidation potential of dopamine (+0.6 V vs Ag/AgCl reference) converted to dopamine concentration using the in vitro calibration of the electrode after the experiment. The electrochemical scans confirmed to be dopamine by the cyclic voltammograms are indicated byopen circles. B, Cyclic voltammograms corresponding to the electrochemical signal at the times indicated by the arrows. The cyclic voltammograms verify that the changes in electrochemical signal during the two transients are attributable to the oxidation of dopamine (middle andright), whereas no changes in dopamine are apparent beforehand (left). The oxidative and reductive peaks of the dopamine transients are compared with those of dopamine obtained during the electrical stimulation of the dopamine fibers (dotted line, scaled to size). C, The video record of the experiment corresponding to the electrochemical signal at the times indicated by the arrows. The first dopamine transient coincided with the entrance of the female to the test chamber and was followed by immediate orientation of the male toward the female. The second transient was concurrent with the initial whisker contact between the rats and was followed by investigative sniffing of the female by the male.

Fig. 5.

Frequency of dopamine concentration transients during brief conspecific episodes: effects of presentation set and conspecific rat. A, Habituation of transients during the second presentation set, by brain region; *p < 0.0001. B, Frequency of transients in the presence of different conspecific rats, by brain region; *p < 0.05, greater than CP nonreceptive female; **p < 0.05, greater than NA male; ^#p < 0.05, greater than NA male, greater than CP nonreceptive female;^##p < 0.05, greater than CP male.

Fig. 6.

Behaviors before and after dopamine concentration transients during conspecific episodes. Left, Behaviors were scored for 5 sec before (white bars) and 5 sec after (gray bars) the start of each dopamine transient; the transient occurred at time 0. The y-axis designates the counts of particular behaviors, with the maximum value considered to be the number of dopamine transients observed in the respective brain region. The x-axis shows seconds before and after the dopamine transient; the z-axis displays various behaviors. Right, The behavior counts from the associated left panels were pooled into before (Pre; white bars) and after (Post; gray bars) totals. Dopamine transients in the CP were significantly associated with increased sniffing of the conspecific. Transients in the NA were significantly associated with increases in general sniffing and orienting movements, as well as approach to and sniffing the conspecific; *p < 0.05, before versus after.

Fig. 7.

Behaviors before and after dopamine concentration transients during copulation episodes. Left, Behaviors were scored for 5 sec before (white bars) and 5 sec after (gray bars) the start of each dopamine transient; the transient occurred at time 0. The y-axis designates the counts of particular behaviors, with the maximum value considered to be the number of dopamine transients observed. Thex-axis shows seconds before and after the dopamine transient, whereas the z-axis displays various behaviors. Right, The behavior counts from the associated left panels were pooled into before (Pre; white bars) and after (Post; gray bars) totals. Dopamine transients were significantly associated with increases in sexual behaviors and with decreases in general sniffing and orienting behaviors; *p < 0.05, before versus after.

Fig. 8.

Histogram of dopamine concentration transients associated with intromissions. The x-axis displays time, with the end of intromission at 0 sec. See Results for operational definitions of mount, thrust, and dismount. The majority of transients occurred before the consummatory aspect of intromission (i.e., thrusting).