Thalamocortical interactions

doi:10.1016/j.conb.2012.03.005

Current Opinion in Neurobiology

Volume 22, Issue 4, August 2012, Pages 575-579

https://doi.org/10.1016/j.conb.2012.03.005 Get rights and content

Glutamatergic pathways dominate information processing in the brain, but these are not homogeneous. They include two distinct types: Class 1, which carries the main information for processing, and Class 2, which serves a modulatory role. Identifying the Class 1 inputs in a circuit can lead to a better understanding of its function. Also, identifying Class 1 inputs to a thalamic nucleus tells us its main function (e.g. the lateral geniculate nucleus, or LGN, is the relay of retinal Class 1 input), and such identification leads to a division of thalamic relays into first and higher order: the former receives Class 1 inputs from subcortical sources; the latter, from layer 5 of cortex, which it then relays to another cortical area. When a cortical area directly connects with another, it often has a parallel, transthalamic connection through these higher order relays. This leads to a novel appreciation of cortical functioning and raises many new questions.

Highlights

► Glutamatergic inputs in thalamic and cortical circuitry are either Class 1 or Class 2. ► We suggest that Class 1 is information bearing and Class 2 is modulatory. ► Class 1 inputs represent what a thalamic nucleus relays to cortex. ► A transthalamic information route exists between cortical areas. ► Many or all cortical areas directly connected have a parallel transthalamic route.

Section snippets

Class 1 and Class 2 glutamatergic inputs

We have made the case in recent years that each glutamatergic pathway participating in thalamic and cortical circuits can be identified as a member of one of two classes, which we now refer to as Class 1 and Class 2 [1, 2]. We originally suggested this classification for thalamic circuitry [3], where we then called them driver (Class 1) and modulator (Class 2) inputs, and we have argued that the Class 1 inputs represent the main information route, whereas the Class 2 inputs serve as modulators

First and higher order thalamic relays

Identifying the Class 1 input to a thalamic nucleus largely defines the function of that nucleus, and so we define the LGN as a relay of retinal input. This logic, in turn, led us to divide the thalamus into two major types: first order and higher order [2, 14]. First order nuclei receive their Class 1 input from a subcortical source, and higher order, from layer 5 of cortex. Higher order thalamic nuclei are thus defined as relaying information between cortical areas.

Identifying Class 1 and 2 inputs in thalamic and cortical circuits

Figure 2a shows the various thalamic and cortical circuits that have been identified as Class 1 or 2. Several points are worth emphasizing:

•
A clear Class 1 (or information bearing) pathway can be followed from layer 5 of one cortical area through a higher order thalamic relay to another cortical area [10•, 12, 13].
•
Cortical areas are also reciprocally connected directly, and these connections involve both Class 1 and 2 inputs in a complex laminar pattern (for details, see [4, 5]).
•
The

Implications for corticocortical processing

If we follow the logic that information is processed mainly by projections of Class 1 glutamatergic inputs, a novel picture emerges for the role of thalamus in corticocortical communications [1, 2, 14]. Figure 3 illustrates some of the main points.

•
A clear information route between cortical areas exists as a transthalamic pathway involving higher order thalamic relays. It appears that often, and perhaps always, when cortical areas have a direct connection, they also have a parallel one through

Conclusions

The idea that glutamatergic pathways are heterogeneous, and that one of the two main classes of such input, Class 1, is the main carrier of information, leads to a novel way of analyzing brain circuits. Other classes may emerge as the classification continues. One of the consequences of this view is that Class 1 inputs define the basic role of a thalamic nucleus, and as such, we can thereby classify these nuclei as first order, if they receive their Class 1 inputs from a subcortical source, and

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgement

The author's laboratory has been supported by grants from the National Institutes of Health.

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View full text

Thalamocortical interactions

Highlights

Section snippets

Class 1 and Class 2 glutamatergic inputs

First and higher order thalamic relays

Identifying Class 1 and 2 inputs in thalamic and cortical circuits

Implications for corticocortical processing

Conclusions

References and recommended reading

Acknowledgement

Visual Neurosci

Distinct functions for direct and transthalamic corticocortical connections

J Neurophysiol

Exploring the Thalamus and its Role in Cortical Function

On the actions that one nerve cell can have on another: distinguishing ‘drivers’ from ‘modulators’

Proc Natl Acad Sci U S A

Synaptic properties of connections between the primary and secondary auditory cortices in mice

Cereb Cortex

Synaptic properties of corticocortical connections between the primary and secondary visual cortical areas in the mouse

J Neurosci

Synaptic properties of thalamic input to the subgranular layers of primary somatosensory and auditory cortices in the mouse

J Neurosci

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

Proc Natl Acad Sci U S A

Synaptic properties of thalamic input to layers 2/3 in primary somatosensory and auditory cortices

J Neurophysiol

Topography and physiology of ascending streams in the auditory tectothalamic pathway

Proc Natl Acad Sci U S A