Ultrastructure and synaptic targets of tectothalamic terminals in the cat lateral posterior nucleus

Kelly, Larry R.; Li, Jianli; Carden, W. Breckinridge; Bickford, Martha E.

doi:10.1002/cne.10800

Cited by 51 publications

(66 citation statements)

References 109 publications

(118 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Likewise, for the visual system, the nature of the tectothalamic pathway from the superior colliculus to pulvinar needs to be determined: Is it a modulator of corticopulvinar-cortical pathways or a parallel visual pathway, or both? Studies in the cat (33) and monkey (34) suggest that these tectal inputs may instead drive pulvinar neurons, implying that prospective differences exist between the visual and auditory systems, and thus may belie a simple canonical principle for organizing the ascending sensory pathways.…”

Section: Discussionmentioning

confidence: 99%

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Lee

Sherman

2009

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Auditory information is relayed from the cochlea along parallel pathways and reaches the inferior colliculus (IC) and the medial geniculate body (MGB) en route to the cortex. Although the ascending tectothalamic pathway to the ventral division of the MGB is regarded as a high-fidelity information-bearing channel, the roles of the pathways to the dorsal and medial divisions are more opaque. Here, we show fundamental differences between these ascending pathways using an in vitro slice preparation. Using photostimulation, we found three main patterns of input (excitatory, inhibitory, and mixed) that differed in each pathway. Furthermore, electrical stimulation of the central nucleus of the IC evoked a depressing response in the MGB with no metabotropic glutamate (mGlu) receptor component, whereas stimulation of the lateral cortex of the IC evoked a facilitating response with an mGlu receptor component. These data suggest that the ascending tectothalamic pathways are functionally distinct from one another.A uditory information ascends from the sensory periphery along parallel pathways, synapsing in the inferior colliculus (IC) and then the medial geniculate body (MGB) en route to the cortex. At the tectothalamic synapse, the IC central nucleus (ICc) reliably transmits excitatory and inhibitory information to the ventral division of the MGB (MGBv) (1, 2). However, the role of the tectothalamic projections from the lateral (ICl), dorsal (ICd), and caudal cortices of the IC [collectively referred to here as the shell region (ICs)] to the dorsal (MGBd) and medial (MGBm) divisions of the MGB are less well understood and may serve either a driving or modulatory role, or both (3, 4). Based on the presence or absence of a cortical layer 5 input, these MGB divisions have been termed first order (MGBv; no layer 5 input) or higher order (MGBd and MGBm; having a layer 5 input), and it is thought that the higher order nuclei play an important role as part of corticothalamocortical circuits (5-7). Previous work in the somatosensory thalamus suggests that the principal driving input to higher order thalamic nuclei arises from this layer 5 input (8). In the auditory system, the anatomical substrates supporting such a driving corticothalamic pathway from layer 5 are also present (6, 7). However, if the cortex provides the principal driving input to the higher order nuclei of the MGB, what is the role of the ascending tectal inputs?Another issue of interest is the observation that auditory tectothalamic inputs are composed of both excitatory and inhibitory pathways. Anatomical studies suggest that the inhibitory feedforward projections to the MGB arise throughout the IC (9, 10), and physiological investigations find several distinct classes of excitatory and inhibitory inputs (11-13). However, the topographic organization of excitatory and inhibitory inputs in the tectothalamic pathways is largely undefined. Are these pathways organized similarly across collicular and thalamic nuclei? Do they align topographically with the anisotropi...

show abstract

Section: Discussionmentioning

confidence: 99%

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Lee

Sherman

2009

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…There are also inferior collicular inputs to the medial division of the medial geniculate nucleus and spinal inputs to the posterior nucleus, raising the possibility that these, too, represent mixed first and higher order relays, but in these cases, it is not yet known if the inferior collicular or spinal inputs to these respective nuclei produce RL terminals. This possibility that these thalamic nuclei putatively identified as higher order may also contain first order relays, as seems the case for the pulvinar (Kelly et al, 2003), does not affect the main conclusion that synapses from driving (RL) ter- Wang et al (2002a). minals are relatively rare in these thalamic nuclei.…”

Section: Drivers Versus Modulatorsmentioning

confidence: 93%

“…Indeed, Kelly et al (2003) have provided clear evidence that there are RL terminals in parts of the pulvinar that are tectal in origin, indicating that the pulvinar complex may include both first and higher order relays. There are also inferior collicular inputs to the medial division of the medial geniculate nucleus and spinal inputs to the posterior nucleus, raising the possibility that these, too, represent mixed first and higher order relays, but in these cases, it is not yet known if the inferior collicular or spinal inputs to these respective nuclei produce RL terminals.…”

Section: Drivers Versus Modulatorsmentioning

confidence: 99%

Fewer driver synapses in higher order than in first order thalamic relays

Horn

Sherman

2007

Neuroscience

View full text Add to dashboard Cite

Abstract-We used electron microscopy to determine the relative numbers of the three synaptic terminal types, RL (round vesicle, large terminal), RS (round vesicles, small terminal), and F (flattened vesicles), found in several representative thalamic nuclei in cats chosen as representative examples of first and higher order thalamic nuclei, where the first order nuclei relay subcortical information mainly to primary sensory cortex, and the higher order nuclei largely relay information from one cortical area to another. The nuclei sampled were the first order ventral posterior nucleus (somatosensory) and the ventral portion of the medial geniculate nucleus (auditory), and the higher order posterior nucleus (somatosensory) and the medial portion of the medial geniculate nucleus (auditory). We found that the relative percentage of synapses from RL terminals varied significantly among these nuclei, these values being higher for first order nuclei (12.6% for the ventral posterior nucleus and 8.2% for the ventral portion of the medial geniculate nucleus) than for the higher order nuclei (5.4% for the posterior nucleus, and 3.5% for the medial portion of the medial geniculate nucleus). This is consistent with a similar analysis of first and higher order nuclei for the visual system (the lateral geniculate nucleus and pulvinar, respectively). Since synapses from RL terminals represent the main information to be relayed, whereas synapses from F and RS terminals are modulatory in function, we conclude that there is relatively more modulation of the thalamic relay in the cortico-thalamo-cortical higher order pathway than in first order relays. © 2007 IBRO. Published by Elsevier Ltd. All rights reserved.Key words: ventral posterior nucleus, posterior nucleus, medial geniculate nucleus, neuromodulators, corticocortical communication. Sherman and Guillery (1998, 2006) first made the point that inputs to thalamic relay cells can be effectively divided into drivers and modulators. A number of features identify driver input, including having powerful, depressing synapses that activate only ionotropic receptors, being the major determinant of receptive field properties of the relay cell, and having singularly large terminals identified with the electron microscope as "RL" (for Round vesicle, Large terminal, and they form symmetric synapses; for details, see Sherman and Guillery, 1998, 2006;Sherman, 2005). A key for this study is that inputs to thalamus terminating in RL, or very large, terminals represent driver inputs. Modulators are associated with weaker, often facilitating synapses that activate ionotropic and metabotropic receptors, and they produce small synaptic terminals. Drivers represent the main information-bearing input to be relayed to cortex and define what is being relayed. For instance, the retinal input is the driver for relay cells of the lateral geniculate nucleus, because it is the retinal input, rather than brainstem or layer 6 cortical input, that represents the main information relayed through the lateral ...

show abstract

“…They found that the ''collicular boutons tend to be larger and distribute to more proximal parts of the dendrites than those from the prefrontal cortex'' and that the SC inputs made asymmetric, excitatory synapses onto the thalamic neurons. While the location of these synapses has to be evaluated in comparison to other structures, such connections close to the soma have also been reported by Kelly et al (2003) in the collicular projection to the pulvinar and lateral posterior nuclei of the cat. Both the physiological and anatomical observations are consistent with the strong driving of MD by the SC and suggests that SC inputs probably have more influence on the MD relay neurons than do cortical inputs.…”

Section: Sc As a Driver Input To MDmentioning

confidence: 93%

Drivers from the deep: the contribution of collicular input to thalamocortical processing

Wurtz

Sommer

Cavanaugh

2005

Progress in Brain Research

View full text Add to dashboard Cite

A traditional view of the thalamus is that it is a relay station which receives sensory input and conveys this information to cortex. This sensory input determines most of the properties of first order thalamic neurons, and so is said to drive, rather than modulate, these neurons. This holds as a rule for first order thalamic nuclei, but in contrast, higher order thalamic nuclei receive much of their driver input back from cerebral cortex. In addition, higher order thalamic neurons receive inputs from subcortical movement-related centers. In the terminology popularized from studies of the sensory system, can we consider these ascending motor inputs to thalamus from subcortical structures to be modulators, subtly influencing the activity of their target neurons, or drivers, dictating the activity of their target neurons? This chapter summarizes relevant evidence from neuronal recording, inactivation, and stimulation of pathways projecting from the superior colliculus through thalamus to cerebral cortex. The study concludes that many inputs to the higher order nuclei of the thalamus from subcortical oculomotor areas -from the superior colliculus and probably other midbrain and pontine regions -should be regarded as motor drivers analogous to the sensory drivers at the first order thalamic nuclei. These motor drivers at the thalamus are viewed as being at the top of a series of feedback loops that provide information on impending actions, just as sensory drivers provide information about the external environment.

show abstract

Ultrastructure and synaptic targets of tectothalamic terminals in the cat lateral posterior nucleus

Cited by 51 publications

References 109 publications

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Fewer driver synapses in higher order than in first order thalamic relays

Drivers from the deep: the contribution of collicular input to thalamocortical processing

Contact Info

Product

Resources

About