Flow of information for emotions through temporal and orbitofrontal pathways

Abstract

The posterior orbitofrontal cortex, anterior temporal sensory association areas and the amygdala have a key role in emotional processing and are robustly interconnected. By analogy with the pattern of connections in early processing sensory areas, anterior temporal sensory and polymodal association cortices send primarily feedforward projections to posterior orbitofrontal cortex and to the amygdala originating in the supragranular layers, in pathways that may provide signals about the external environment. The amygdala innervates all layers of the posterior orbitofrontal cortex, including the middle, or feedforward, target layers, in a pathway that may convey information about emotional context. The posterior orbitofrontal cortex targets dual systems in the amygdala which have opposite effects on central autonomic structures. Both pathways originate in posterior orbitofrontal cortex, but one targets heavily the inhibitory intercalated masses, whose activation can ultimately disinhibit central autonomic structures during emotional arousal. The other pathway innervates the central nucleus of the amygdala, and can lead to downstream inhibition of central autonomic structures, resulting in autonomic homeostasis. The choice of pathway may depend on emotional context, and probably involves other prefrontal areas, including lateral prefrontal areas, which have executive functions. Lateral prefrontal cortices issue feedforward projections that target layer 5 of orbitofrontal cortex, which is the chief output layer to the amygdala. These laminar-specific pathways suggest sequential and collaborative interactions in evaluating the sensory and emotional aspects of the environment for decision and action in complex behaviour.

Fig. 1

Cortical types in the orbitofrontal and anterior temporal region. (A) Shades of grey depict cortical type, with agranular areas shaded in the darkest grey. Progressively lighter shades of grey show dysgranular and granular (eulaminate) cortices. Cortical areas (without delineation of their borders) are indicated by numbers. O, before architectonic areas refers to orbital. Abbreviations: OPAll, orbital periallocortex (agranular cortex); OPro, orbital proisocortex (dysgranular type); TE, inferior temporal visual association area (eulaminate cortex); sts, superior temporal sulcus. (B) Cartoon showing the broad laminar features of different types of cortex. Two types of eulaminate cortices are depicted, differing in the density of granular layer 4 and in the density of the supragranular layers 2–3. Note that orbitofrontal cortex does not have areas with the type of cortex depicted on the far right, found only on the lateral surface of the prefrontal cortex.

Fig. 2

Laminar patterns of corticocortical connections. (A) Projection neurons from earlier-processing sensory areas originate in the supragranular layers and their axons terminate mostly in the middle–deep layers of later-processing sensory areas, and are called feedforward (red). Projections proceeding in the reverse direction originate in the deep layers and their axons terminate mostly in the upper layers, especially layer 1 of earlier-processing areas, and are called feedback (blue). (B) Limbic cortices (which are either agranular or dysgranular in type) issue projections mostly from their deep layers, and their axons terminate most densely in layer 1 of association areas, akin to feedback projections, regardless of the direction of projections.

Fig. 3

The varied patterns of laminar terminations linking prefrontal cortices. (A) Dark-field photomicrograph of coronal section through the centre of the orbitofrontal cortex of a rhesus monkey brain showing terminations of axons (white grain) forming a column in orbitofrontal area 13 (white arrowhead), with denser termination in layer 1. (B) Axonal terminations forming three modules restricted to the deep layers of the cortex in the lateral bank of the upper limb of the arcuate sulcus.

Fig. 4

The laminar pattern of connections in a limbic area of orbitofrontal cortex. (A) Bright-field photomicrograph shows the architecture of a limbic orbitofrontal area, which has fewer than six distinguishable layers. (B) Dark-field photomicrograph shows that when this limbic area projects to a eulaminate association area the majority of projections neurons (white neurons) are found in the deep layers (5–6) and fewer are found in the upper layers (2–3). Adapted from Barbas (1986).

Fig. 5

The microenvironment of projections originating and terminating in different layers varies. Model of corticocortical projections, using as an example projections from prefrontal cortex to temporal cortex, indicating that projections originating in layer 3 (left) and terminating in the middle layers (right) encounter an environment that differs from projections originating in the deep layers (left) and terminating in layer 1 (right). The model shows specifically the differences in the microenvironment with respect to inhibitory neurons at the site of termination (right). The neurochemical class of parvalbumin inhibitory neurons (depicted in black) are most prevalent in the middle cortical layers, and innervate the proximal dendrites or axon initial segment of neighbouring neurons. Axons terminating in layer 1 encounter a microenvironment where the neurochemical class of calbindin inhibitory neurons are most prevalent (depicted in grey), which innervate the distal dendrites of neighbouring neurons.

Fig. 6

Feedforward projections from the upper layers of anterior temporal polymodal cortices project to the amygdala. (A) Cross-section through the entorhinal and perirhinal cortex showing projection neurons (small arrows) found mostly in the upper layers in the lateral bank of the rhinal sulcus (R) after injection of biotinylated dextran amine (BDA) in the basal nuclei of the amygdala. These projection neurons that are directed to the amygdala are found mostly in layer 3 of polymodal area 36, within the lateral bank of the rhinal sulcus, and in visual association area TE1, situated more laterally in the inferior temporal cortex. The section was counterstained with Nissl. (B) An adjacent unstained section shows the same pattern of projections to the amygdala from the above areas (arrows). Note that projection neurons in the entorhinal cortex (area 28), a limbic area, situated medial to the rhinal sulcus, are found in layer 5. Medial is to the left.

Fig. 7

Posited sequence of information processing for emotions. Temporal sensory association cortex issues mostly feedforward projections to the amygdala (F, pathway t), and the amygdala issues projections to orbitofrontal cortex (A) terminating in complex laminar patterns (not shown), including substantial feedforward projections to the middle layers (pathway a). The orbitofrontal cortex (A, basal part) has bidirectional and highly specific connections with the amygdala (F), originating robustly from layer 5 and directed to the intercalated masses of the amygdala (pathway o, green branch), and to the basal nuclei of the amygdala (pathway o, black branch). Projections to the intercalated masses influence the internal processing of the amygdala, by inhibiting the central (Ce) nucleus (small red arrow) and thus disinhibiting its output to autonomic structures in the hypothalamus (B), brainstem and the spinal cord (C, D, E). Projections from layer 5 of orbitofrontal cortex are also directed to hypothalamic autonomic centres (B, pathway o2), which is linked with brainstem and spinal autonomic centres (C, D, E). Activation of these pathways would be expected to accompany emotional arousal. Another pathway from orbitofrontal cortex to the central nucleus of the amygdala (o1) would inhibit hypothalamic autonomic centres (long red arrow), leading to autonomic homeostasis. Decision for action in emotional situations may ultimately be directed from lateral prefrontal cortices, which innervate the middle–deep layers of orbitofrontal cortices, including layer 5 (pathway l), according to the rules of the structural model for connections (top, left). Layer 5 of orbitofrontal cortex is the chief output to the amygdala (pathways o, or o1). Black or green arrows show excitatory pathways. Red arrows show inhibitory pathways.