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Alex M Thomson

Publications and source records attributed to Alex M Thomson.

11 recordsLinked to original sources

Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs.

The properties of the connections made by the axons of pyramidal cells with cortico-thalamic (CT)-like morphology with a range of postsynaptic layer 6 targets were studied with dual intracellular recordings in slices of adult rat and cat neocortex. The cells were filled with biocytin and identified morphologically and, where appropriate, immunofluorescently. CT-like pyramids contacted interneurons with a very high probability (up to 1:2) but contacted other layer 6 pyramidal cells only rarely (approximately 1:80). The excitatory postsynaptic potentials (EPSPs) that they elicited both in pyramidal cells and in a variety of types of interneurons (including those immunopositive for parvalbumin and for somatostatin) facilitated, the second EPSP being larger than the first over a range of interspike intervals. Facilitation was not, however, maximal at the shortest intervals; in fact, depression was apparent at some connections at short interspike intervals. Facilitation in the majority of connections peaked at intervals of 25-35 ms and then declined slowly. Nor did these connections display the augmentation typical of many other strongly facilitating connections. Third EPSPs were smaller on average than second EPSPs, and fourth and subsequent EPSPs could be depressed (relative to first EPSPs). The properties of the outputs of these CT-like pyramidal cells are therefore quite distinct from those of other pyramidal cells, both within layer 6 and in other layers, possibly reflecting their unique role as both first order thalamo-cortical recipient and cortico-thalamic output neurons.

Adaptation, Physiological↗

Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex.

Paired intracellular recordings with biocytin labelling were made in slices of adult rat somatosensory and visual cortex and in cat visual cortex to examine the properties of synaptic connections made by layer 6 pyramidal cells, to determine whether cortico-cortical pyramids more commonly provide input to other layer 6 pyramids than cortico-thalamic cells, and whether these connections exhibit paired pulse and brief train depression. Pyramidal cells with cortico-cortical like morphology were 2-4 times more likely to innervate other pyramidal cells than were cortico-thalamic like cells, but less likely to innervate inhibitory interneurons. The excitatory postsynaptic potentials elicited by presynaptic, phasically firing cortico-cortical pyramids in all classes of postsynaptic infragranular layer pyramidal cells exhibited strong, presynaptically mediated paired pulse and brief train depression. Those with larger paired pulse ratios also exhibited post-tetanic potentiation, but this was accompanied by stronger paired pulse and brief train depression. Both the firing characteristics and the outputs of cortico-cortical pyramidal cells display pronounced phasic characteristics, indicating that these cells respond most effectively to and preferentially pass on information related to novelty.

Animals↗

Excitatory and inhibitory connections show selectivity in the neocortex.

The cerebral cortex is pivotal in information processing and higher brain function and its laminar structure of six distinct layers, each in receipt of a different constellation of inputs, makes it important to identify connectivity patterns and distinctions between excitatory and inhibitory pathways. The 'feedforward' projections from layer 4-3 and from 3-5 target pyramidal cells and to lesser degrees interneurones. 'Feedback' projections from layer 5-3 and from 3-4, on the other hand, mainly target interneurones. Understanding the microcircuitry may give some insight into the computation and information processing performed in this brain region.

Animals↗

Interlaminar connections in the neocortex.

This review summarizes the local circuit, interlaminar connections in adult mammalian neocortex. These were first demonstrated with anatomical techniques, which indicate some of the exquisite spatial precision present in the circuitry. Details, such as the class(es) of neurons targeted by some of these projections, have begun to be added in studies that combine paired/triple intracellular recordings with dye-filling of connected neurons. Clear patterns are emerging from these studies, with 'forward' projections from layer 4 to 3 and from 3 to 5 targeting both selected pyramidal cells and interneurons, while 'back' projections from layer 5 to 3 and from 3 to 4 target only interneurons. To place these data in a wider context, the major afferent inputs to and efferent outputs from each of the layers are discussed first.

Afferent Pathways↗

Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex.

Using dual intracellular recordings in slices of adult rat and cat neocortex, the frequency-filtering characteristics of 'depressing' synapses made by pyramidal axons at interspike intervals between 5 and 50 ms were studied. At 'depressing' connections from excitatory cells to some inhibitory interneurons (n = 6), recovery from short interspike interval depression was near exponential. Extrapolation of exponentials fitted to this recovery demonstrated a residual 10-20% depression at intervals >50 ms. This slowly decaying component was larger for later excitatory postsynaptic potentials (EPSPs) in trains which were typically more strongly depressed. At >80% of connections between spiny excitatory cells and at pyramid to parvalbumin-immunopositive interneuron connections, however, recovery exhibited a more complex time course. A narrow 'notch' (half-width 5 ms), peaking at intervals of 13-25 ms during which the EPSP was depressed further, interrupted recovery from short interval depression. This 'notch' was equally apparent for all EPSPs in brief trains and was mediated presynaptically.

Action Potentials↗

Target and temporal pattern selection at neocortical synapses.

We attempt to summarize the properties of cortical synaptic connections and the precision with which they select their targets in the context of information processing in cortical circuits. High-frequency presynaptic bursts result in rapidly depressing responses at most inputs onto spiny cells and onto some interneurons. These 'phasic' connections detect novelty and changes in the firing rate, but report frequency of maintained activity poorly. By contrast, facilitating inputs to interneurons that target dendrites produce little or no response at low frequencies, but a facilitating-augmenting response to maintained firing. The neurons activated, the cells they in turn target and the properties of those synapses determine which parts of the circuit are recruited and in what temporal pattern. Inhibitory interneurons provide both temporal and spatial tuning. The 'forward' flow from layer-4 excitatory neurons to layer 3 and from 3 to 5 activates predominantly pyramids. 'Back' projections, from 3 to 4 and 5 to 3, do not activate excitatory cells, but target interneurons. Despite, therefore, an increasing complexity in the information integrated as it is processed through these layers, there is little 'contamination' by 'back' projections. That layer 6 acts both as a primary input layer feeding excitation 'forward' to excitatory cells in other layers and as a higher-order layer with more integrated response properties feeding inhibition to layer 4 is discussed.

Action Potentials↗

Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus.

To investigate the electrophysiological properties, synaptic connections, and anatomy of individual parvalbumin-immunoreactive (PV-IR) and cholecystokinin-immunoreactive (CCK-IR) interneurones in CA1, dual intracellular recordings using biocytin-filled microelectrodes in slices of adult rat hippocampus were combined with fluorescence labelling of PV- and CCK-containing cells. Of 36 PV-IR cells, 29 were basket cells, with most of their axonal arbours in the stratum pyramidale (SP). Six were bistratified cells with axons ramifying throughout stratum oriens (SO) and stratum radiatum (SR). One was a putative axo-axonic cell with an axonal arbour confined to half of the SP and a narrow adjacent region of the SO. Of 27 CCK-IR neurones, 13 were basket cells, with most of their axonal arbours in the SP, and included basket cells with somata in the SP (6), SO (3), and SR (2) and at the border between the stratum lacunosum-moleculare (SLM) and the SR (2). In addition, several dendrite-targeting cell classes expressed CCK-IR: 4 of 9 bistratified cells with axons ramifying in the SO and SR; all five Schaffer-associated cells whose axons ramified extensively in the SR; both cells classified as quadrilaminar because their axons ramified in the SO, SP, SR, and SLM; one SO-SO cell whose dendritic and axonal arbours were contained within the SO; and one perforant path-associated cell with axonal and dendritic arbours within the distal SR and SLM. The majority (31 of 36) of PV-IR neurones recorded were fast-spiking, and most fast-spiking cells tested (25 of 29 basket, 1 axo-axonic, and 5 of 6 bistratified cells) were PV-IR. However, 1 of 6 regular-spiking basket, 1 of 4 regular-spiking bistratified, and 3 of 5 burst-firing basket cells were also PV-IR. In contrast, the majority (17 of 27) of the CCK-IR neurones recorded were regular-spiking, 3 were burst-firing, and 7 were fast-spiking. These data confirm that the majority of PV-IR and CCK-IR axon terminals innervate proximal portions of CA1 pyramidal cells. Most PV-IR cells are fast-spiking, whereas most CCK-IR cells are regular-spiking. In both neurochemical classes basket cells predominate, but both groups included subpopulations of dendrite-targeting cells. Despite these similarities, the two populations exhibited very different somatic distributions, and each contained cellular morphologies not represented in the other.

Action Potentials↗

Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro.

Dual and triple intracellular recordings with biocytin labelling in slices of adult neocortex explored small circuits of synaptically connected neurons. 679 paired recordings in rat and 319 in cat yielded 135 and 42 excitatory postsynaptic potentials (EPSPs) and 37 and 26 inhibitory postsynaptic potentials (IPSPs), respectively. Patterns of connectivity and synaptic properties were similar in the two species, although differences of scale and in the range of morphologies were observed. Excitatory 'forward' projections from layer 4 to 3, like those from layer 3 to 5, targeted pyramidal cells and a small proportion of interneurons, while excitatory 'back' projections from layer 3 to 4 selected interneurons, including parvalbumin immuno-positive basket cells. Layer 4 interneurons that inhibited layer 3 pyramidal cells included both basket cells and dendrite-targeting cells. Large interneurons, resembling cells previously described as large basket cells, in layers 4 and 3 (cat), with long myelinated horizontal axon collaterals received frequent excitatory inputs from both layers. A very high rate of connectivity was observed between pairs of interneurons, often with quite different morphologies, and the resultant IPSPs, like the EPSPs recorded in interneurons, were brief compared with those recorded in pyramidal and spiny stellate cells.

Animals↗

Selectivity in the inter-laminar connections made by neocortical neurones.

In this brief review of inter-laminar synaptic connections in neocortex a case is made for the hypothesis that axons select their targets, or neurones select their inputs with great specificity. A large part of the data discussed was obtained from dual intracellular recordings in slices of adult neocortex. The neurones innervated in a given layer by a given type of axon were not found to be a random selection of the cells in that layer. Rather in a layer to layer specific fashion, certain types of target cells are densely innervated while others are not contacted or receive only weak inputs. In another layer, the same axons may select other targets.

Animals↗

Presynaptic frequency- and pattern-dependent filtering.

Dual intracellular recordings from pairs of synaptically connected neurones have demonstrated that the frequency-dependent pattern of transmitter release varies dramatically between different classes of connections. Somewhat surprisingly, these patterns are not determined by the class of neurone supplying the axon alone, but to a large degree by the class of postsynaptic neurone. A wide range of presynaptic mechanisms, some that depress the release of transmitter and others that enhance release have been identified. It is the selective expression of these different mechanisms that determines the unique frequency- and pattern-dependent properties of each class of connection. Although the molecular interactions underlying these several mechanisms have yet to be fully identified, the wealth and complexity of the protein-protein and protein-lipid interactions that have been shown to control the release of transmitter suggest many ways in which the properties of a synapse may be tuned to respond to particular patterns and frequencies.

Animals↗