Distribution of GABAergic cells in the inferior colliculus that project to the thalamus.
inhibition; auditory system; GAD; medial geniculate; tectothalamic
A GABAergic component has been identified in the projection from the inferior colliculus (IC) to the medial geniculate body (MG) in cats and rats. We sought to determine if this GABAergic pathway exists in guinea pig, a species widely used in auditory research. The guinea pig IC contains GABAergic cells, but their relative abundance in the IC and their relative contributions to tectothalamic projections are unknown. We identified GABAergic cells with immunochemistry for glutamic acid decarboxylase (GAD) and determined that \textasciitilde21% of IC neurons are GABAergic. We then combined retrograde tracing with GAD immunohistochemistry to identify the GABAergic tectothalamic projection. Large injections of Fast Blue, red fluorescent beads or FluoroGold were deposited to include all subdivisions of the MG. The results demonstrate a GABAergic pathway from each IC subdivision to the ipsilateral MG. GABAergic cells constitute \textasciitilde22% of this ipsilateral pathway. In addition, each subdivision of the IC had a GABAergic projection to the contralateral MG. Measured by number of tectothalamic cells, the contralateral projection is about 10% of the size of the ipsilateral projection. GABAergic cells constitute about 20% of the contralateral projection. In summary, the results demonstrate a tectothalamic projection in guinea pigs that originates in part from GABAergic cells that project ipsilaterally or contralaterally to the MG. The results show similarities to both rats and cats, and carry implications for the role of GABAergic tectothalamic projections vis-a-vis the presence (in cats) or near absence (in rats and guinea pigs) of GABAergic interneurons in the MG.
Mellott Jeffrey G; Foster Nichole L; Nakamoto Kyle T; Motts Susan D; Schofield Brett R
Frontiers in neuroanatomy
2014
1905-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnana.2014.00017" target="_blank" rel="noreferrer noopener">10.3389/fnana.2014.00017</a>
Cholinergic and non-cholinergic projections from the pedunculopontine and laterodorsal tegmental nuclei to the medial geniculate body in Guinea pigs.
GABA; auditory; thalamus; sleep; acetylcholine; arousal; glutamate
The midbrain tegmentum is the source of cholinergic innervation of the thalamus and has been associated with arousal and control of the sleep/wake cycle. In general, the innervation arises bilaterally from the pedunculopontine tegmental nucleus (PPT) and the laterodorsal tegmental nucleus (LDT). While this pattern has been observed for many thalamic nuclei, a projection from the LDT to the medial geniculate body (MG) has been questioned in some species. We combined retrograde tracing with immunohistochemistry for choline acetyltransferase (ChAT) to identify cholinergic projections from the brainstem to the MG in guinea pigs. Double-labeled cells (retrograde and immunoreactive for ChAT) were found in both the PPT (74%) and the LDT (26%). In both nuclei, double-labeled cells were more numerous on the ipsilateral side. About half of the retrogradely labeled cells were immunonegative, suggesting they are non-cholinergic. The distribution of these immunonegative cells was similar to that of the immunopositive ones: more were in the PPT than the LDT and more were on the ipsilateral than the contralateral side. The results indicate that both the PPT and the LDT project to the MG, and suggest that both cholinergic and non-cholinergic cells contribute substantially to these projections.
Motts Susan D; Schofield Brett R
Frontiers in neuroanatomy
2010
2010
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnana.2010.00137" target="_blank" rel="noreferrer noopener">10.3389/fnana.2010.00137</a>
Subcollicular projections to the auditory thalamus and collateral projections to the inferior colliculus.
superior olive; medial geniculate nucleus; binaural; brain evolution; lateral lemniscus; paralemniscal area; parallel pathways; reticular formation
Experiments in several species have identified direct projections to the medial geniculate nucleus (MG) from cells in subcollicular auditory nuclei. Moreover, many cochlear nucleus cells that project to the MG send collateral projections to the inferior colliculus (IC) (Schofield et al., 2014). We conducted three experiments to characterize projections to the MG from the superior olivary and the lateral lemniscal regions in guinea pigs. For experiment 1, we made large injections of retrograde tracer into the MG. Labeled cells were most numerous in the superior paraolivary nucleus, ventral nucleus of the trapezoid body, lateral superior olivary nucleus, ventral nucleus of the lateral lemniscus, ventrolateral tegmental nucleus, paralemniscal region and sagulum. Additional sources include other periolivary nuclei and the medial superior olivary nucleus. The projections are bilateral with an ipsilateral dominance (66%). For experiment 2, we injected tracer into individual MG subdivisions. The results show that the subcollicular projections terminate primarily in the medial MG, with the dorsal MG a secondary target. The variety of projecting nuclei suggest a range of functions, including monaural and binaural aspects of hearing. These direct projections could provide the thalamus with some of the earliest (i.e., fastest) information regarding acoustic stimuli. For experiment 3, we made large injections of different retrograde tracers into one MG and the homolateral IC to identify cells that project to both targets. Such cells were numerous and distributed across many of the nuclei listed above, mostly ipsilateral to the injections. The prominence of the collateral projections suggests that the same information is delivered to both the IC and the MG, or perhaps that a common signal is being delivered as a preparatory indicator or temporal reference point. The results are discussed from functional and evolutionary perspectives.
Schofield Brett R; Mellott Jeffrey G; Motts Susan D
Frontiers in neuroanatomy
2014
1905-7
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnana.2014.00070" target="_blank" rel="noreferrer noopener">10.3389/fnana.2014.00070</a>
Projections from auditory cortex to cholinergic cells in the midbrain tegmentum of guinea pigs.
Animals; Auditory Cortex/*metabolism; Auditory Pathways/metabolism; Axonal Transport; Axons/metabolism; Choline O-Acetyltransferase/*metabolism; Efferent Pathways/metabolism; Female; Fluorescent Antibody Technique; Guinea Pigs; Immunohistochemistry; Male; Neurons/*metabolism; Tegmentum Mesencephali/*metabolism
Anterograde and retrograde tracing techniques were used to characterize projections from the auditory cortex to the pedunculopontine and laterodorsal tegmental nuclei (PPT and LDT, respectively) in the midbrain tegmentum in guinea pigs. For anterograde tracing, tetramethylrhodamine dextran (FluoroRuby) was injected at several sites within auditory cortex. After sufficient time for transport, the brain was processed for immunohistochemistry with anti-choline acetyltransferase to reveal presumptive cholinergic cells. Anterogradely labeled axons were observed ipsilaterally and, in smaller numbers, contralaterally, in both the pedunculopontine and laterodorsal tegmental nuclei. In all four nuclei, tracer-labeled boutons appeared to contact immunolabeled (i.e., cholinergic) cells. The contacts occurred on cell bodies and dendrites. The results were similar following injections that spread across multiple auditory cortical areas or injections that were within primary auditory cortex. In order to confirm the anterograde results, in a second series of experiments, retrograde tracers were deposited in the pedunculopontine tegmental nucleus. These injections labeled layer V pyramidal cells in the auditory cortex. The results suggest an excitatory projection from primary auditory cortex bilaterally to cholinergic cells in the midbrain tegmentum. Such a pathway could allow auditory cortex to activate brainstem cholinergic circuits, possibly including the cholinergic pathways associated with arousal and gating of acoustic stimuli.
Schofield Brett R; Motts Susan D
Brain research bulletin
2009
2009-09
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.brainresbull.2009.06.015" target="_blank" rel="noreferrer noopener">10.1016/j.brainresbull.2009.06.015</a>
Cholinergic cells of the pontomesencephalic tegmentum: connections with auditory structures from cochlear nucleus to cortex.
Acetylcholine/metabolism; Animals; Auditory Cortex/pathology; Auditory Pathways; Axons/physiology; Cholinergic Agents/*metabolism; Cholinergic Fibers/*metabolism; Cochlear Nucleus/*physiology; Cognition Disorders; Guinea Pigs; Humans; Neurotransmitter Agents/metabolism; Prosencephalon/pathology; Rats; Tegmentum Mesencephali/metabolism/*physiology
Acetylcholine (ACh) is a neuromodulator that is likely to play a role in plasticity as well as other phenomena at many sites in the auditory system. The auditory cortex receives cholinergic innervation from the basal forebrain, whereas the cochlea receives cholinergic innervation from the superior olivary complex. Much of the remainder of the auditory pathways receives innervation from the pedunculopontine and laterodorsal tegmental nuclei, two nuclei referred to collectively as the pontomesencephalic tegmentum (PMT). The PMT provides the major source of ACh to the auditory thalamus and the midbrain, and is a substantial source (in addition to the superior olivary complex) of ACh in the cochlear nucleus. Individual cholinergic cells in the PMT often have axon branches that innervate multiple auditory nuclei, including nuclei on both sides of the brain as well as nuclei at multiple levels of the auditory system. The auditory cortex has direct axonal projections to the PMT cells, including cholinergic cells that project to the inferior colliculus or cochlear nucleus. The divergent projections of PMT cholinergic cells suggest widespread effects on the auditory pathways. These effects are likely to include plasticity as well as novelty detection, sensory gating, reward behavior, arousal and attention. Descending projections from the forebrain, including the auditory cortex, are likely to provide a high level of cognitive input to these cholinergic effects. Dysfunction associated with the cholinergic system may play a role in disorders such as tinnitus and schizophrenia.
Schofield Brett R; Motts Susan D; Mellott Jeffrey G
Hearing research
2011
2011-09
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.heares.2010.12.019" target="_blank" rel="noreferrer noopener">10.1016/j.heares.2010.12.019</a>
Projections from the dorsal and ventral cochlear nuclei to the medial geniculate body.
thalamus; collateral projections; fear conditioning; lemniscal pathway; magnocellular pathway; multimodal processing; multipolar cells; T-stellate
Direct projections from the cochlear nucleus (CN) to the medial geniculate body (MG) mediate a high-speed transfer of acoustic information to the auditory thalamus. Anderson etal. (2006) used anterograde tracers to label the projection from the dorsal CN (DCN) to the MG in guinea pigs. We examined this pathway with retrograde tracers. The results confirm a pathway from the DCN, originating primarily from the deep layers. Labeled cells included a few giant cells and a larger number of small cells of unknown type. Many more labeled cells were present in the ventral CN (VCN). These cells, identifiable as multipolar (stellate) or small cells, were found throughout much of the VCN. Most of the labeled cells were located contralateral to the injection site. The CN to MG pathway bypasses the inferior colliculus (IC), where most ascending auditory information is processed. Anderson etal. (2006) hypothesized that CN-MG axons are collaterals of axons that reach the IC. We tested this hypothesis by injecting different fluorescent tracers into the MG and IC and examining the CN for double-labeled cells. After injections on the same side of the brain, double-labeled cells were found in the contralateral VCN and DCN. Most double-labeled cells were in the VCN, where they accounted for up to 37% of the cells labeled by the MG injection. We conclude that projections from the CN to the MG originate from the VCN and, less so, from the DCN. A significant proportion of the cells send a collateral projection to the IC. Presumably, the collateral projections send the same information to both the MG and the IC. The results suggest that T-stellate cells of the VCN are a major source of direct projections to the auditory thalamus.
Schofield Brett R; Motts Susan D; Mellott Jeffrey G; Foster Nichole L
Frontiers in neuroanatomy
2014
1905-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fnana.2014.00010" target="_blank" rel="noreferrer noopener">10.3389/fnana.2014.00010</a>