Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey

An anatomical approach to possible areas in the cerebral cortex involved in somatic motor behavior is to analyze the cortical areas containing neurons that connect directly to the primary motor cortex (MI). To define the cortical areas related to orofacial movements, we examined the distribution of cortical neurons that send their axons to the orofacial region of the MI in the macaque monkey. Injections of retrograde tracers into the electrophysiologically identified orofacial region of the MI revealed that labeled neurons were distributed in the following cortical areas: the orbital cortex (area 12), insular cortex, frontoparietal operculum (including the deep part of the cortical masticatory area and the secondary somatosensory cortex), ventral division of the premotor cortex (especially in its lateral part), orofacial region of the supplementary motor area, rostral division of the cingulate motor area (CMA), and CMA on the ventral bank. A number of labeled neurons were also seen in the MI around the injection sites and in the parietal cortex (including the primary somatosensory cortex and area 7b). No labeled neurons were found in the dorsal division of the premotor cortex. Fluorescent retrograde double labeling further revealed virtually no overlap of distribution between cortical neurons projecting to the orofacial and forelimb regions of the MI. Based on the present results, we discuss the functional diversity of the cortical areas related to orofacial motor behavior and the somatotopical organization in the premotor areas of the frontal cortex. J. Comp. Neurol. 389:34–48, 1997.© 1997 Wiley-Liss, Inc.     

Anatomical and physiological properties of the projection from the sensory cortex to the motor cortex in normal cats: the difference between corticocortical and thalamocortical projections

Details of the distribution of terminal sites of the projection fibers from area 2 of the sensory cortex to the motor cortex were studied and compared with the distribution of terminals from the ventrolateral (VL) nucleus of the thalamus to the motor cortex. The results obtained were as follows: Intracortical microstimulation (ICMS) in area 2 produced measurable short-latency EPSPs only in neurons located in layers II and III of the motor cortex, whereas VL stimulation produced short-latency EPSPs in neurons throughout the depths of the motor cortex. The time from the beginning to the peak of the EPSPs was not significantly different for area 2- and VL-elicited EPSPs suggesting that there was no systematic difference between effective terminal sites for both inputs. However, there was a difference when a given neuron received both inputs suggesting that there was a segregation between the two inputs within a given cell. The majority of area 2-elicited EPSPs were smooth and monophasic, but some (40%) of them showed double peaks indicating that some neurons received mono- and disynaptic inputs from area 2. Intracellular injections of HRP suggested that neurons receiving input from area 2 were predominantly multipolar non-pyramidal neurons in layers II and III whereas neurons receiving thalamic input were pyramidal as well as non-pyramidal cells. Field potentials in the motor cortex evoked by area 2 stimulation did not change polarity in the depths of the cortex and therefore, differed from the VL-evoked potentials suggesting differences in the mechanisms of generating the electrical fields. It is concluded that association fibers effective for producing EPSPs terminate primarily on non-pyramidal cells in layer II and III whereas VL fibers terminate not only on pyramidal but also on non-pyramidal cells in layers III and V. This study provided a basis for examining the modifiability of association fibers after elimination of VL input to the motor cortex which is reported in the following paper.     

Primary motor cortex receives input from area 3a in macaques

Intracortical microstimulation was used to define topographic sectors and the rostral border of primary motor cortex in adult macaques (Macaca mulatta). In the same animals, injections of fluorescent tracers were made within defined regions of primary motor cortex. Retrogradely labeled neurons were topographically distributed in area 3a, with most neurons located in layer III, and fewer neurons situated in layers V and IV. These findings suggest that muscle afferent information, thought to be important in a closed-loop mode of function, may reach primary motor cortex directly from cortical area 3a.     

Microstimulation in auditory cortex provides a substrate for detailed behaviors

Sensory cortical prostheses have potential to aid people suffering from blindness, deafness and other sensory deficits. However, research to date has shown that sensation thresholds via epicortical stimulation are surprisingly large. These thresholds result in potentially deleterious electrical currents, as well as large activation volumes. Large activation volumes putatively limit the corresponding number of independent stimulation channels in a neural prosthesis. In this study, penetrating stimulation of the auditory cortex was tested for its ability to transmit salient information to behaving rat subjects. Here, we show that subjects that were previously trained to discriminate natural stimuli immediately discriminated different microstimulation cues more accurately and with shorter response latencies than the natural stimuli. Additionally, the cortical microstimulation resulted in a generalization gradient across locations within the cortex. The results demonstrate the efficacy of using closely spaced cortical microstimulation to efficiently transmit highly salient and discriminable information to a behaving subject.     

Preserved ipsilateral-to-lesion motor map organization in the unilateral 6-OHDA-treated rat model of Parkinson's disease

The classic view of dopamine (DA) loss in Parkinson's disease is that it produces a functional deafferentation in striatal-cortical circuitry that, in turn, contributes to sensorimotor deficits. The present study examines this view in the rat by assessing how DA-depletion affects the intracortical microstimulation (ICMS) topographic representation of movement in the rostral and caudal motor areas of the motor cortex. The ICMS map is used as an index of motor cortex function because it has been shown to reflect motor function and experience. Groups of rats received no training or skilled reach training and were then given unilateral 6-hydroxydopamine (6-OHDA) or sham lesions of the nigrostriatal bundle to deplete nigrostriatal DA. Lesion success was confirmed by abnormalities in skilled reaching, by apomorphine-induced rotation, and by loss of DA neurons in the substantia nigra. The size and threshold of the motor map in naive and skilled reach trained DA-depleted rats were preserved. In addition, there was an increase in distal limb representation in the caudal forelimb area (CFA) in the DA-depleted rats suggesting a possible plastic response to the behavioral effects of DA-depletion. The presence of preserved size and modified map organization in DA-depleted rats is discussed in relation to the hypothesis that preserved motor cortex functionality despite DA loss underlies the spared motor abilities of DA-depleted rats.     

Is the hindlimb representation of the rat''s cortex a ‘sensorimotor amalgam’?

In the rat, the hindlimb representation of the sensorimotor cortex is characterized by the presence of large pyramids in the fifth layer and a dense granular layer ('sensorimotor amalgam'). The objective was to investigate in the rat, whether or not the efferent zones to the gastrocnemius muscle and the proprioceptive feedback projection from that muscle to the cortex are co-extensive. To this end, the proprioceptive zone was mapped by means of field potentials and single unit discharges evoked by controlled longitudinal displacements of the gastrocnemius tendon. The efferent zones to the gastrocnemius muscle were mapped by means of intracortical microstimulation (ICMS; less than 30 microA). The proprioceptive zone occupied a territory extending from 1.0 to 2.5 mm caudal to the bregma and from 2.0 to 3.0 mm lateral from the midline. The response properties were similar to those observed previously in area 3a of monkeys. For sinusoidal displacements threshold amplitude decreased with increasing stretch frequency. The modal value of response latency was 7 ms, the shortest latency 4 ms. The ICMS zone lay 0.5 to 1.5 mm caudal to bregma having an overlap of 0.5 mm with the proprioceptive region. The proprioceptive as well as the motor areas lay within the granular cortex, but overlapped only to a small extent.     

Pattern of pyramidal tract collateralization to medial thalamus,lateral hypothalamus and red nucleus in the cat

Summary Stimulating electrodes were placed in the red nucleus, lateral hypothalamus and medial thalamus in order to determine whether pyramidal tract (PT) neurons send collaterals to those sites. The red nucleus projections are well-known, but it was discovered that PT neurons also project into the other two sites. All of the fibers that sent collaterals to all three sites originated from fast PT neurons. Those that responded to stimulation of the skin and that sent collaterals to two or three sites were predominantly fast PT neurons. Those neurons that responded only to cerebral peduncle stimulation were predominantly slowly-conducting, when compared with the set of PT neurons in response to cerebral peduncle stimulation. The patterns of collateral branching to red nucleus and to lateral hypothalamus were similar, suggestimg a similar synaptic effect of the pyramidal system in the two sites. Measurement of the speed of conduction from three sites along the length of corticospinal fibers revealed large changes on some, but not all, fibers; there was no evident pattern to these changes that might be associated with collateral branching. A new hypothesis concerning the functional role of fast PT neurons in regulating movement is presented.Dr. Canedo was supported by a Fogarty International Research Fellowship     

Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons

Frontal eye field (FEF) projections to the midbrain and pons were studied in nine macaque monkeys that were used to study FEF projections to the striatum and thalamus (Stanton et al.: J. Comp. Neurol. 271:473-492, '88). Injections of tritiated amino acids or WGA-HRP were made into FEF cortical locations where low-level microstimulation (less than or equal to 50 microA) elicited saccadic eye movements, and anterograde axonal labeling was mapped. The injections were made into the anterior bank of the arcuate sulcus from dorsomedial sites where large saccades were evoked (lFEF) to ventrolateral sites where small saccades were evoked (sFEF). The largest terminal fields of FEF fibers were located in the ipsilateral superior colliculus (SC). Projections to SC were topographically organized: lFEF sites projected to intermediate and deep layers of caudal SC, sFEF sites projected to intermediate and superficial layers of rostral SC, and FEF sites between these extremes projected to intermediate locations in SC. Patches of terminal labeling were located ipsilaterally in the lateral mesencephalic reticular formation near the parabigeminal nucleus and the ventrolateral pontine reticular formation. These patches were larger from lFEF injections. Small, dense terminal patches were seen in the ipsilateral pontine gray, mostly along the medial and dorsal borders of these nuclei but occasionally in central and dorsolateral regions. Patches of label like those in the pontine nuclei were located ipsilaterally in the reticularis tegmenti pontis nucleus in lFEF cases and bilaterally in sFEF cases. Small terminal patches were found in the nucleus of Darkschewitsch and dorsal and medial parts of the parvicellular red nucleus in most FEF cases. In the pretectal region, labeled terminal patches were consistently found in the nucleus limitans of the posterior thalamus, but we could not determine if label in the nucleus of the pretectal area and dorsal parts of the nucleus of the posterior commissure marked axon terminals or fibers of passage. We found small, lightly labeled terminal patches in the pontine raphe between the rootlets of the abducens nerve (three cases) or in the adjacent paramedian pontine reticular formation (one case). Omnipauser cells in this region are important in initiating saccades. In one sFEF case, very small patches of label were located in the supragenual nuclei anterior to the abducens nuclei and in the ipsilateral nucleus prepositus hypoglossi posterior to the abducens nucleus. Presaccadic burster neurons in the periabducens region are known to fire immediately before horizontal saccades.(ABSTRACT TRUNCATED AT 400 WORDS)     

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Microstimulation mapping identified vocalization areas in primate anterior cingulate cortex. Rat anterior cingulate and medial prefrontal areas have also been intensely investigated, but we do not know, how these cortical areas contribute to vocalizations and no systematic mapping of stimulation‐evoked vocalizations has been performed. To address this question, we mapped microstimulation‐evoked (ultrasonic) vocalizations in rat cingulate and medial prefrontal cortex. The incidence of evoked vocalizations differed markedly between frontal cortical areas. Vocalizations were most often evoked in posterior prelimbic cortex and cingulate area 2, whereas vocalizations were rarely evoked in dorsal areas (vibrissa motor cortex, secondary motor cortex and cingulate area 1) and anterior areas (anterior prelimbic, medial‐/ventral‐orbital cortex). Vocalizations were observed at intermediate frequencies in ventro‐medial areas (infralimbic and dorsopeduncular cortex). Various complete, naturally occurring calls could be elicited. In prelimbic cortex superficial layer microstimulation evoked mainly fear calls with low efficacy, whereas deep layer microstimulation evoked mainly 50 kHz calls with high efficacy. Vocalization stimulation thresholds were substantial (70–500 μA, the maximum tested; on average ~400 μA) and latencies were long (median 175 ms). Posterior prelimbic cortex projected to numerous targets and innervated brainstem vocalization centers such as the intermediate reticular formation and the nucleus retroambiguus disynaptically via the periaqueductal gray. Anatomical position, stimulation effects and projection targets of posterior prelimbic cortex were similar to that of monkey anterior cingulate vocalization cortex. Our data suggest that posterior prelimbic cortex is more closely involved in control of vocalization initiation than in specifying acoustic details of vocalizations.