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Emotional Flow - Review Article: Barbas 2007

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Page covers selected thoughts from article Flow of information for emotions.

Article Review

Abstract

• key role in emotional processing:
  • HCA/anterior temporal sensory association areas (ATS)
  • BGA/amygdala (AM)
  • ACA/posterior orbitofrontal cortex (OPFC)
• ATS and polymodal association cortices send primarily feedforward projections to OPFC
  • originate in supragranular layers
  • provide signals about external environment
• AM innervates all layers of OPFC
  • convey information about emotional context
• OPFC targets dual systems in amygdala which have opposite effects on central autonomic structures
  • to AM/inhibitory intercalated masses -> disinhibit central autonomic structures during emotional arousal
  • to AM/central nucleus -> autonomic homeostasis
  • depend on emotional context
• lateral prefrontal cortices (LPFC) issue feedforward projections to target layer 5 of OPFC, which is chief output layer to AM
• sequential and collaborative interactions
  • evaluating the sensory and emotional aspects of the environment
  • decision and action in complex behaviour

Introduction

• prefrontal cortex (PFC)
  • receives information from most of cerebral cortex and subcortical structures
  • handles only relevant task information at one time
• choosing relevant information
  • must be conducted within emotional context that helps focus attention
  • we can handle common things automatically but alerted by some signals
  • article considers pathways of selective attention for emotional events among 3 structures - ATS, AM, OPFC
• ATS robustly interlinked in tiad pathways with both OPFC and AM
  • integrate information on sensory features and emotional significance of events

Architecture of orbitofrontal cortex

• each PFC area has unique architectonic features - size and the shape of neurons in individual layers
  • e.g. giant Betz cells in layer 5 characterize primary motor cortex
• cortical type refers to broad structural features - number of layers, width and density of layer 4, overall neuronal density
  • unifies architectonically different areas into groups by common features
  • OPFC areas belong to 1-3 cortical types defined by number of layers
• best descriptor of cortical type in PFC is layer 4 neural density - from agranular (lowest density) to granular (highest density)
• another descriptor is distribution of PV and CB inhibitory neurons
  • agranular - highest CB, lowest PV
  • granular - average CB, PV
  • type 3 is most granular cortex type in OPFC
  • type 4 is in LPFC
• caudal OPFC (OPAll, OFap)
  • samples entire sensory periphery through cortical connections
  • has strongest connections with limbic structures that process signals on the internal environment
  • has most robust and specialized connections with AM

Caudal OPFC has view of external and internal environments

• Caudal OPFC has polymodal nature
  • connections with cortices of each and every sensory modality, including visual, auditory, somatosensory, gustatory and olfactory
  • only rhinal/perirhinal region (part of HCA) has comparable richness
• OPFC receives highly processed sensory data from ATS
• OPFC reciprocates with ATS
• responses of OPFC neurons to sensory stimuli are closely linked to reward contingencies and not strictly to their physical properties
  • if monkeys learn that red stimulus signifies reward and green stimulus does not, OPFC neurons respond to red stimulus
  • when reward contingencies are later reversed, same neurons respond to green stimulus
• OPFC has strong bidirectional links with limbic structures
  • anterior cingulate (PFC/CG)
  • AM/BGA, HC/HCA, MD/THA
  • limbic structure provide internal, emotional information to OPFC

Laminar pattern of connections

Sensory cortices as model systems

• OPFC has bidirectional connections with ATS
• topography does not answer what is processing sequence, but clues are in processing in early sensory areas
  • sensory signal goes to thalamus -> primary sensory cortex -> association cortices
  • sensory signal is relayed via thalamus nuclei to level 4 and around of primary sensory cortex as feedforward connections
  • primary sensory cortex projects (from upper layers, mostly layer 3) in feedforward manner to association areas
  • thus, when corticocortical projection is away from sensor and from layer 3 to layer 4, then it is feedforward
• corticocortical projections from sensory association areas back to primary sensory cortex are feedback projections
  • originate in the deep layers (5–6)
  • terminate most densely in layer 1 (where apical dendrites located)
• can we use analogy?
  • pattern of connections between high-order association cortices is quite complex, originating and terminating in varying proportions in different cortical layers
  • nevertheless, these complex patterns have consistent laminar organization that can be explained within the context of cortical type

Cortical type underlies laminar pattern of corticocortical connections

• cortical limbic areas have common overall structure, being either agranular or dysgranular in type
• connections from limbic cortices to association cortices are feedback projections in sensory systems
• cortical type can best predict laminar pattern of connections
  • laminar structure changes gradually and systematically across cortical region
  • changes can be described quantitatively by number of layers, overall neuronal density and distribution of PV, CB neurons
  • there is clear trend: projection neurons from given area originate in upper layers and their axons terminate in middle–deep layers (4–6) of areas with fewer layers or lower neuronal density than cortex of origin
  • opposite connections, from areas with fewer layers or lower neuronal density, originate in deep layers and their axons terminate in upper layers (1–3) of areas with either more layers or higher neuronal density
• dependency of patterns of connections from cortical type is named structural model
  • proportion of upper-to-deep axon terminals varies accordingly to relative difference in structure
  • when areas of similar type are interconnected, pattern of terminations in each cortex is columnar, encompassing all cortical layers, and projection neurons originate in roughly equal numbers in layers 2–3 and 5–6

The functional significance of laminar-specific connections

• laminar-specific connections have implications for function
  • axons terminating in upper layers influence different populations of neuronal elements than axons terminating in deep layers
  • key laminar-specific difference is in the predominant classes of inhibitory neurons
  • PV (black) is expressed in basket and chandelier cells in middle layers of cortex, synapse with neighbouring pyramidal neurons, by innervating their proximal dendrites and axon initial segments
  • CB-positive inhibitory neurons (gray) include double bouquet neurons in cortex, prevalent in cortical layer 2 and upper layer 3, and innervate distal dendrites and spines of neighbouring neurons
• prefrontal axons that terminate in different layers are also synaptically distinct
  • boutons from prefrontal axons synapsing in the superficial layers of superior temporal cortex are smaller in size and contain fewer synaptic vesicles than boutons terminating in middle cortical layers
  • relationship of bouton size to laminar terminations holds for boutons from axons originating in distinct prefrontal areas and terminating in same temporal area, or originating in same prefrontal area and terminating in different superior temporal cortices

Laminar-specific pathways for emotions

Feedforward projections from temporal sensory areas reach OPFC

• granular temporal visual or auditory association cortices issue projections to caudal OPFC in feedforward manner
• feedback axons originating in dysgranular OPFC terminate in upper layers of granular anterior temporal area TE
• axons from same OPFC target middle to deep layers of agranular temporal cortex
• majority of terminations from axons originating in dysgranular area 36, which is polymodal, terminate in middle to deep layers of agranular OPFC in feedforward manner

Sequential feedforward projections from sensory cortices to AM and to OPFC

• neurons from ATS project in feedforward manner to OPFC
• same parts ATS that project to OPFC project to AM
• OPFC receives direct projections from ATS, and potentially indirect projections from sensory cortices through AM
• next pathway is from AM to OPFC, which terminates in complex pattern involving all layers
  • includes significant projections from AM that target middle layers of limbic PFC, especially caudal OPFC
  • there is a ‘feedforward’ projection from polymodal and unimodal ATS to the AM, and a ‘feedforward’ projection from AM to OPFC
• feedforward projections from ATS cortices reach OPFC
• there is potential indirect route from ATS to OPFC through AM
• connections of OPFC and ATS overlap extensively in AM

Specialized linkage of OPFC with AM

• posterior OPFC has multimodal and highly ordered laminar-specific connections with ATS cortices
• caudal OPFC have strong and bidirectional connections with AM
• posterior OPFC cortices are distinguished among PFC for their specialized connections with AM
  • most striking specialization is partial segregation of input and output connections in AM that link it with posterior OPFC
  • projection neurons from AM directed to OPFC originate most densely from basolateral, basomedial (accessory basal) and lateral nuclei, and to lesser extent in cortical nuclei of AM
  • reciprocal projections from caudal OPFC terminate in basal complex of AM, and to lesser extent in central and cortical nuclei of AM
• axons from posterior OPFC target most heavily intercalated masses (IM) of AM, small GABAergic neurons between different nuclei of AM
  • IM do not project to cortex, but have significant connections within AM, project to and inhibit central nucleus of AM
  • central nucleus issues inhibitory projections to HT/BSA
  • activation of OPFC pathway to IM result in disinhibition of HT/BSA and activate spinal autonomic structures in emotional arousal
• HT/BSA receive direct innervation from OPFC, but even stronger innervation from caudal MPFC/ACA in anterior CG/ACA
• lighter pathway from caudal OPFC goes to central nucleus of AM
  • when this pathway is activated, expected inhibition of HT/BSA and prevent its excitatory influence on spinal autonomic centers

Who decides on action

• Black or green arrows show excitatory pathways. Red arrows show inhibitory pathways.
• ATS cortex issues feedforward projections to AM (F, pathway t), and AM issues projections to OPFC (A) terminating in complex laminar patterns (not shown), including substantial feedforward projections to the middle layers (pathway a)
• OPFC (A, basal part) has bidirectional and highly specific connections with AM (F), originating robustly from layer 5 and directed to IM/AM (pathway o, green branch), and to basal nuclei of AM (pathway o, black branch)
  • projections to IM inhibit central (Ce) nucleus (small red arrow) and thus disinhibits its output to HT/BSA (B) and the spinal cord (C, D, E)
  • another pathway from OPFC to central nucleus of AM (o1) inhibits HT/BSA (long red arrow), leading to autonomic homeostasis
• projections from layer 5 of OPFC are directed to HT/BSA (B, pathway o2), which is linked with BSA and spinal autonomic centres (C, D, E)
• decision for action in emotional situations may ultimately be directed from LPFC, which innervate the middle–deep layers of OPFC, including layer 5 (pathway l), according to rules of the structural model for connections (top, left). Layer 5 of OPFC is chief output to AM (pathways o, or o1).
• caudal LPFC have connections with PMC - decision can be translated into action

• signals from LPFC to OPFC would have to be specific, signalling activation of either OPFC pathway to IM/AM in sounding general alarm (pathway o), or a pathway from OPFC to central nucleus of AM for return to autonomic homeostasis (pathway o1, dotted line)
• mechanism for selection of each pathway is unknown