Response properties of single units in areas of rat auditory thalamus that project to the amygdala

Projections from the auditory thalamus to the amygdala have been implicated in the processing of the emotional signficance of auditory stimuli. In order to further our understanding of the contribution of thalamoamygdala projections to auditory emotional processing, acoustic response properties of single neurons were examined in the auditory thalamus of chloral hydrate-anesthetized rats. The emphasis was on the medial division of the medial geniculate body (MGm), the suprageniculate nucleus (SG), and the posterior intralaminar nucleus (PIN), thalamic areas that receive inputs from the inferior colliculus and project to the lateral nucleus of the amygdala (AL). For comparison, recordings were also made from the specific thalamocortical relay nucleus, the ventral division of the medial geniculate body (MGv). Responses latencies were not statistically different in MGv, MGm, PIN, and SG, but were longer in the posterior thalamic region (PO). Overall, frequency tuning functions were narrower in MGv than in the other areas but many cells in MGm were as narrowly tuned as cells in MGv. There was some organization of MGv, with low frequencies represented dorsally and high frequencies ventrally. A similar but considerably weaker organization was observed in MGm. While the full range of frequencies tested (1–30 kHz) was represented in MGv, cells in MGm, PIN, and SG tended to respond best to higher frequencies (16–30 kHz). Thresholds were higher in PIN than in MGv (other areas did not differ from MGv). Nevertheless, across the various areas, the breadth of tuning was inversely related to threshold, such that more narrowly tuned cells tended to have lower thresholds. Many of the response properties observed in MGm, PIN, and SG correspond with properties found in AL neurons and thus add support to the notion that auditory responses in AL reflect thalamoamygdala transmission.     

Discharge properties of MST neurons that project to the frontal pursuit area in macaque monkeys

We have used antidromic activation to determine the functional discharge properties of neurons that project to the frontal pursuit area (FPA) from the medial-superior temporal visual area (MST). In awake rhesus monkeys, MST neurons were considered to be activated antidromically if they emitted action potentials at fixed, short latencies after stimulation in the FPA and if the activation passed the collision test. Antidromically activated neurons (n = 37) and a sample of the overall population of MST neurons (n = 110) then were studied during pursuit eye movements across a dark background and during laminar motion of a large random-dot texture and optic flow expansion and contraction during fixation. Antidromically activated neurons showed direction tuning during pursuit (25/37), during laminar image motion (21/37), or both (16/37). Of 27 neurons tested with optic flow stimuli, 14 showed tuning for optic flow expansion (n = 10) or contraction (n = 4). There were no statistically significant differences in the response properties of the antidromically activated and control samples. Preferred directions for pursuit and laminar image motion did not show any statistically significant biases, and the preferred directions for eye versus image motion in each sample tended to be equally divided between aligned and opposed. There were small differences between the control and antidromically activated populations in preferred speeds for laminar motion and optic flow; these might have reached statistical significance with larger samples of antidromically activated neurons. We conclude that the population of MST neurons projecting to the FPA is highly diverse and quite similar to the general population of neurons in MST.     

Response characterstics of spinothalamic tract neurons that project to the posterior thalamus in rats

A sizeable number of spinothalamic tract axons terminate in the posterior thalamus. The functional roles and precise areas of termination of these axons have been a subject of recent controversy. The goals of this study were to identify spinothalamic tract neurons (STT) within the cervical enlargement that project to this area, characterize their responses to mechanical and thermal stimulation of their receptive fields, and use microantidromic tracking methods to determine the nuclei in which their axons terminate. Forty-seven neurons were antidromically activated using low-amplitude (< or =30 microA) current pulses in the contralateral posterior thalamus. The 51 points at which antidromic activation thresholds were lowest were surrounded by ineffective tracks indicating that the surrounded axons terminated within the posterior thalamus. The areas of termination were located primarily in the posterior triangular, medial geniculate, posterior and posterior intralaminar, and suprageniculate nuclei. Recording points were located in the superficial and deep dorsal horn. The mean antidromic conduction velocity was 6.4 m/s, a conduction velocity slower than that of other projections to the thalamus or hypothalamus in rats. Cutaneous receptive fields appeared to be smaller than those of neurons projecting to other areas of the thalamus or to the hypothalamus. Each of the examined neurons responded exclusively or preferentially to noxious stimuli. These findings indicate that the STT carries nociceptive information to several target nuclei within the posterior thalamus. We discuss the evidence that this projection provides nociceptive information that plays an important role in fear conditioning.     

Vibrissa-responsive neurons of the superior colliculus that project to the intralaminar thalamus of the rat

Responses to deflection of vibrissae were studied in neurons of the superior colliculus projecting to the intralaminar thalamus. Forty-two percent were activated by deflection of several vibrissae. Some units showed habituation and directional sensitivity but no other feature extraction was noted. All responsive units were located in the intermediate and deep layers in a roughly somatotopic distribution and intermingled with other projecting and non-projecting units.     

Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys

Surprisingly little is known about the proportions of projections of different areas and regions of neocortex to the superior colliculus in primates. To obtain an overview of such projection patterns, we placed a total of 10 injections of retrograde tracers in the superior colliculus of three New World monkeys (Callithrix, Callicebus, and Aotus). Because cortex was flattened and cut parallel to the surface, labeled corticotectal neurons could be accurately located relative to architectonic boundaries and surface features. While there was variability across cases and injection sites, the summed results clearly support several conclusions. One, three well-defined visual areas, V1 (18%), V2 (14%), and MT (11%), contributed nearly half of the total of labeled cells. Two, several other visual areas (V3, DL, DM, and FST) that are early in the processing hierarchy provided another fifth of the total. Three, inferior temporal visual areas of the ventral stream provided only minor projections. Four, visuomotor fields (FEF, FV, cortex in the region of SEF, and posterior parietal cortex) contained less than 10% of the labeled neurons. Five, few labeled neurons were in auditory or somatosensory areas. The results indicate that cortical inputs to the superior colliculus originate predominantly from early visual areas rather than from multimodal or visuomotor areas.     

Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey.

1. Thalamic neurons that receive synaptic input from the globus pallidus or the cerebellar nuclei were identified in awake monkeys trained to perform an arm-reaching task. The location of electrophysiologically identified cerebellar-receiving (CR) and pallidal-receiving (PR) neurons was used to identify a total of 264 thalamic neurons in cerebellar (CB) or pallidal (GP) regions of the thalamus. 2. Stimulation in the brachium conjunctivum or white matter adjacent to the cerebellar nuclei excited 85 neurons in the thalamus at short latencies. These CR neurons were located in the oral portion of the ventral posterolateral nucleus (VPLo), in caudal portions of the ventral lateral nucleus (VLc), and in area X. 3. Stimulation in the internal globus pallidus (GPi) inhibited 10 thalamic neurons at short latency. These PR neurons were located in rostral portions of VLc, in the oral part of the ventral lateral nucleus (VLo), and in the parvicellular part of the ventral anterior nucleus (VApc). 4. There was no clear single somatotopic organization of neurons in CB and GP regions of the thalamus, as defined by "free-form" responses to passive manipulation and observation of eye movements. There was, in fact, a tendency for two representations, each, of the head/eye/mouth cells and cells with modifications of activity in response to manipulation of the arm. 5. During the hold period before illumination of a visual target, the mean firing rates and variability of discharge of arm-related CR and PR neurons did not differ significantly. This was also true for the total sample of arm-related neurons in the CB versus GP regions. 6. The activity of many neurons in both the CB and GP regions began to change before the reaching movement and, for some, before the earliest recorded changes in electromyographic (EMG) activity. The initial change was an increase in discharge for greater than 75% of the cells studied in both the CB and GP regions. 7. During the reaching task, there also was no significant difference in the time of the initial change in discharge of neurons in the CB versus GP regions of the thalamus. 8. These data are consistent with the hypothesis that the initial task-related change in discharge of PR thalamic neurons is dominated by input from the cerebral cortex and that pallidal input modulates later phases of their movement-related changes in activity.     

Single pallidal neurons project both to the striatum and thalamus in the rat

Collateral projections of single small pallidal neurons to the striatum and paraventricular nucleus of the thalamus were observed in the rat using a fluorescent retrograde double labeling technique. This population of pallidal cells was almost separate from the more predominant pallidal cell group projecting to the subthalamic nucleus. We propose that the globus pallidus proper might have the same two functionally distinct populations (limbic and motor), that have been well documented in the striatum and entopeduncular nucleus.     

Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys

The goal of the present neuroanatomical study in macaque monkeys was twofold: (1) to clarify whether the hand representation of the primary motor cortex (M1) has a transcallosal projection to M1 of the opposite hemisphere; (2) to compare the topography and density of transcallosal connections for the hand representations of M1 and the supplementary motor area (SMA). The hand areas of M1 and the SMA were identified by intracortical microstimulation and then injected either with retrograde tracer substances in order to label the neurons of origin in the contralateral motor cortical areas (four monkeys) or, with an anterograde tracer, to establish the regional distribution and density of terminal fields in the opposite motor cortical areas (two monkeys). The main results were: (1) The hand representation of M1 exhibited a modest homotopic callosal projection, as judged by the small number of labeled neurons within the region corresponding to the contralateral injection. A modest heterotopic callosal projection originated from the opposite supplementary, premotor, and cingulate motor areas. (2) In contrast, the SMA hand representation showed a dense callosal projection to the opposite SMA. The SMA was found to receive also dense heterotopic callosal projections from the contralateral rostral and caudal cingulate motor areas, moderate projections from the lateral premotor cortex, and sparse projections from M1. (3) After injection of an anterograde tracer (biotinylated dextran amine) in the hand representation of M1, only a few small patches of axonal label were found in the corresponding region of M1, as well as in the lateral premotor cortex; virtually no label was found in the SMA or in cingulate motor areas. Injections of the same anterograde tracer in the hand representation of the SMA, however, resulted in dense and widely distributed axonal terminal fields in the opposite SMA, premotor cortex, and cingulate motor areas, while labeled terminals were clearly less dense in M1. It is concluded that the hand representations of the SMA and M1 strongly differ with respect to the strength and distribution of callosal connectivity with the former having more powerful and widespread callosal connections with a number of motor fields of the opposite cortex than the latter. These anatomical results support the proposition of the SMA being a bilaterally organized system, possibly contributing to bimanual coordination.On leave from the Institute of Physiology, Armenian Academy of Sciences, Erevan, Armenia     

Functional properties of dorsal horn neurons that project to the dorsal accessory olive

1. This study examined the responses to natural cutaneous stimuli of neurons in the dorsal horn of the lumbosacral spinal cord that project to the dorsal accessory portion of the inferior olive (DAO) in cats anesthetized with pentobarbital sodium. Extracellular activity was recorded from single units antidromically activated by currents of less than or equal to 70 muA applied to DAO. 2. A total of 119 antidromically activated neurons was examined. Their antidromic activation latencies displayed a wide range (2.5-24.6 ms). The average latency corresponds to a conduction velocity of 24 m/s. 3. Collision was demonstrated for 24 neurons. All responded to some form of natural cutaneous stimulation. Their receptive fields encompassed some portion of the hind limb, particularly the toes; one-third displayed gradients of sensitivity. 4. Based on their thresholds to peripheral stimulation, the 24 neurons fell into five categories, those sensitive to light cutaneous stimuli (i.e., hair movement or light touch; 37.5%), rub (21%), tap (21%), pressure (12.5%), or noxious stimuli (8%). 5. Comparison of these results with data on the other major source of somatosensory information for DAO, the gracile nucleus (examined previously with the same methods), suggests that the sensitivity of neurons in DAO to light cutaneous stimuli is mediated primarily by neurons in the dorsal horn. The sensitivity of neurons in DAO to tap, rub, or pressure, on the other hand, might be mediated by neurons in either the dorsal horn, the gracile nucleus, or both.     

Sensorimotor transformations in cortical motor areas

A central problem in motor research has been to understand how sensory signals are transformed to generate a goal-directed movement. This problem has been formulated as a set of coordinate transformations that begins with an extrinsic coordinate frame representing the spatial location of a target and ends with an intrinsic coordinate frame describing muscle activation patterns. Insight into this process of sensorimotor transformation can be gained by examining the coordinate frames of neuronal activity in interconnected regions of the brain. We recorded the activity of neurons in primary motor cortex (M1) and ventral premotor cortex (PMv) in a monkey trained to perform a task which dissociates three major coordinate frames of wrist movement: muscle, wrist joint, and an extrinsic coordinate frame. We found three major types of neurons in M1 and PMv. The first type was termed 'extrinsic-like'. The activity of these neurons appeared to encode the direction of movement in space independent of the patterns of wrist muscle activity or joint movement that produced the movements. The second type was termed 'extrinsic-like with gain modulation'. The activity of these neurons appeared to encode the direction of movement in space, but the magnitude (gain) of neuronal activity depended on the posture of the forearm. The third type was termed 'muscle-like' since their activity co-varied with muscle activity. The great majority of the directionally-tuned neurons in the PMv were classified as 'extrinsic-like' (48/59, 81%). A smaller group was classified as 'extrinsic-like with gain modulation' (7/59, 12%). In M1, the three types of neurons were more equally represented. Our results raise the possibility that cortical processing between M1 and PMv may contribute to a sensorimotor transformation between extrinsic and intrinsic coordinate frames. Recent modeling studies have demonstrated the computational plausibility of such a process.     

Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord. I. Electrophysiological properties of pyramidal neurons

To study cortical motor control, we examined electrical characteristics of pyramidal neurons in the present report, and intra- or juxta-columnar connections of the pyramidal neurons to corticospinal neurons in the accompanying report. Pyramidal neurons were intracellularly recorded and stained in slices of rat motorsensory cortices (areas FL, HL and M1) where many corticospinal neurons were labeled retrogradely. They were morphologically classified into classical, star and other modified pyramidal neurons, and electrophysiologically into regular-spiking (RS), intrinsic bursting (IB) and irregular-spiking (IS) neurons on the basis of spiking pattern in response to 500 ms depolarizing current pulses. RS responses were further divided into RS with slow adaptation (RS-SA) and RS with fast adaptation (RS-FA). The electrical properties were associated with the laminar location of the neurons; RS-SA responses were observed frequently in layer II/III and less frequently in layers IV–VI, and IB and IS responses were exclusively found in layers V and VI, respectively. Interestingly, all layer IV neurons in area FL/HL were RS-FA star-pyramidal neurons, whereas layer IV neurons in area M1 were RS-SA classical pyramidal neurons. Although weak stimulation of areas FL/HL and M1 is known to elicit movement, these results suggest different information processings between the two areas.     

Neurons of the acoustic thalamus that project to the amygdala contain glutamate.

Injection of WGA-HRP into the lateral nucleus of the amygdala produced retrograde axonal transport to cell bodies in areas of the acoustic thalamus: the medial division of the medial geniculate body, the suprageniculate nucleus, and the posterior intralaminar nucleus. Glutamate-immunoreactive neurons were present throughout the acoustic thalamus, including the regions containing the retrogradely labeled neurons. Many of the retrogradely labeled cells were also immunoreactive for glutamate. Thus, glutamate is present in those neurons of the acoustic thalamus that project to the amygdala and may contribute to neurotransmission and synaptic plasticity in this pathway.     

The distribution and some morphological features of substantia nigra neurons that project to the thalamus,superior colliculus and pedunculopontine nucleus in the monkey

Neurons of the substantia nigra's pars reticulata that send axons to the thalamus, superior colliculus and midbrain reticular formation (including the pedunculopontine nucleus) have been revealed in monkeys by the technique of retrograde transport of horseradish peroxidase. The populations of nigrothalamic, nigrotectal and nigroreticular neurons differ from one another in their number, intranigral distribution and somatodendritic size and shape. Nigrothalamic cells are the most abundant and, although scattered throughout the mediolateral expanse of the pars reticulata, their numbers progressively diminish from rostral to caudal levels. Nigrotectal cells are least numerous and are restricted almost exclusively to the lateral margin of the rostral one-half of the pars reticulata. Nigroreticular cells, like nigrothalamic, are scattered throughout the mediolateral dimension of the nucleus, but are more commonly located at middle to caudal levels. In addition to their restricted intranigral location, the nigrotectal cells are larger, polygonal and have more major dendritic processes than the smaller nigrothalamic and nigroreticular cells which are usually triangular or fusiform. A small proportion of cells of all three types appears to project contralaterally.These findings indicate that the efferent organization of the primate pars reticulata differs markedly from that of the rodent¹⁸ and the monkey's nigrotectal cells constitute a spatially and morphologically distinct subpopulation within the pars reticulata. These data should be useful in understanding the functional organization of topographic inputs to the pars reticulata such as that from the neostriatum.     

A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds

The pallido-recipient thalamus transmits information from the basal ganglia to the cortex and is critical for motor initiation and learning. Thalamic activity is strongly inhibited by pallidal inputs from the basal ganglia, but the role of nonpallidal inputs, such as excitatory inputs from cortex, remains unclear. We simultaneously recorded from presynaptic pallidal axon terminals and postsynaptic thalamocortical neurons in a basal ganglia-recipient thalamic nucleus that is necessary for vocal variability and learning in zebra finches. We found that song-locked rate modulations in the thalamus could not be explained by pallidal inputs alone and persisted following pallidal lesion. Instead, thalamic activity was likely driven by inputs from a motor cortical nucleus that is also necessary for singing. These findings suggest a role for cortical inputs to the pallido-recipient thalamus in driving premotor signals that are important for exploratory behavior and learning.     

Context-dependent force coding in motor and premotor cortical areas

In three monkeys trained to finely grade grip force in a visuomotor step-tracking task, the effect of the context on neuronal force correlates was quantitatively assessed. Three trial types, which differed in force range, number, and direction of the force steps, were presented pseudo-randomly and cued with the color of the cursor serving as feedback of the exerted force. Quantitative analyses were made on 85 neurons with similar discharge patterns in the three trial types and significant linear positive (54 cells) or negative (31 cells) correlation coefficients between firing rate and force. An analysis of covariance (ANCOVA) showed that the population slopes for 2-step were steeper than for 3-step trials. Another ANCOVA at the population level, computed on the differences in firing rate and force between force steps, persistently disclosed a significant effect of trial type. For the first two force steps, the differences in firing rate were significantly larger in the 2-step than in the 3-step increase trials. Further analyses revealed that neither the force range nor the number of steps was a unique factor. A small group of neurons was tested in an additional trial series with a uniform cue for all three trials, leading to either a loss of context-dependency or to unexpected changes in firing rate. This demonstrates that the cue color was an important instruction for task performance and neuronal activity. The most important findings are that the context-dependent changes were occurring ”on-line”, and that neurons displaying context-dependency were found in all three lateral premotor cortex hand regions and in the primary motor cortex. Finger muscle activity did not show any context dependency. The context-dependent effect leads to a normalization of the cortical activity. The advantage of normalization is discussed and mechanisms for the gain regulation are proposed. Received: 10 November 1998 / Accepted: 13 March 1999     

Changes in the cortical silent period after repetitive magnetic stimulation of cortical motor areas

Behavioral experiments were conducted to examine the role of the cholinergic receptor-agonist muscarine or its antagonist homatropine on the mating behavior of sexually experienced male rats. Male copulatory behavior was recorded after intrathecally administered saline, muscarine (7.5 μg), or homatropine (25 μg). Changes in copulatory behavior were assessed by the following parameters: intromission latency, intromission frequency, intercopulatory interval, ejaculation latency, and postejaculatory interval. Intromission frequency, intercopulatory interval, and ejaculation latency were decreased significantly by muscarine. Intrathecal homatropine decreased the number of copulating animals (five out of 13). In the five animals that were able to ejaculate after homatropine, intromission latency, intercopulatory interval, and ejaculation latency increased significantly. The effects of both drugs on locomotion were also tested. Muscarine induced no significant changes in locomotion compared with saline. A significant increase in locomotion was found after homatropine treatment. These results suggest that acetylcholine, acting at spinal-cord muscarinic receptors, may be involved in ejaculation. Electronic Publication