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1

introduction

see notes

• Motor and somatosensory cortex close together - interact/have functional links
• Thalamus - gateway for sensory info - interacts with cortex
• Cerebellum - coords diff actions
• Basal ganglia - interconnected in sensory and motor pathway - deep in brain - subcortical area like thalamus - central function - connectivity's
• Many interactions happening
• Complex cerebral network seems to be involved in sensory-motor integration, inc. sensorimotor cerebral cortex, basal ganglia and cerebellum
• Cortical frontal and parietal areas strongly interconnected and function together for many aspects of action planning
• Starting from sensory parietal areas, primary somatosensory cortex (S1) consists of postcentral gyrus of parietal lobe, which corresponds to Brodmann areas 3a, 3b, 1, 2
• Axons from thalamic neurons receiving somatic sensations terminate in somatotopically corresponding regions of S1
• S1 projects to secondary somatosensory cortex (SII), located on superior border of lateral fissure
• Posterior parietal cortex (PPC) involved in spatial attention, spatial awareness and multisensory integration (Colby and Goldberg, 1999)
• Recent studies suggest that PPC plays imp role in diff action-related functions, inc. movement intention (together with frontal areas; Andersen & Buneo, 2002)
- PPC crucial node for sensory-motor integration, in that it integrates extrinsic (from 'external' world) and intrinsic (from body) sensory inputs in order to create cognitive representation of movement for motor planning and understanding

2

Similarities between the song system and mammalian motor behaviour pathways (Nottebohm, 2005)

• HVC projects to nucleus RA directly (PDP), and indirectly via Area X, the dorsolateral anterior thalamic nucleus (DLM), and LMAN (AFP)
• Shares similarities with mammalian pathway cortex --> basal ganglia --> thalamus --> cortex

see notes

3

Similarities between the song system and mammalian motor behaviour pathways (Nottebohm, 2005) research

There is a tradition in biology of using specific animal models to study generalizable basic properties of a system. For example, the giant axon of squid was used for the pioneering work on nerve transmission; the fruit fly (Drosophila) has played a key role in researchers discovering the role of homeobox genes in embryogenesis; the sea slug (Aplysia) is used to study the molecular biology of learning; and the round worm (Caenorhabditis elegans) is used to study programmed cell death. Basic insights gained from these four systems apply widely to other multicellular animals. Here, I will review basic discoveries made by studying birdsong that have helped answer more general questions in vertebrate neuroscience

4

Basal ganglia modulate motor outputs and action selection (Smeets et al., 2000)

• Tetrapod vertebrates share a common pattern of basal ganglia (BG) organisation and connectivity in striato-pallidal systems
• Shared chemical markers: dopamine, substance P and enkephalin
• Further similarities in devel and expression of homeobox (Hox) genes (reg genes that control devel in all multicellular organisms, from fungi-humans)
- Mammals have dramatic increase of projections from cortex (pallium) in processing of thalamic sensory info from diff modalities relayed to BG - role extends beyond motor control to inc also cog, emotional, and sensorimotor functions (via loops that have reciprocal connections with frontal, limbic and sensory systems)

see notes

• Dorsal and ventral striatopallidal systems
• The dorsal and ventral striatopallidal systems.
• The basal ganglia are organised into dorsal and ventral striatopallidal systems in all tetrapods.
• For each vertebrate class, 2 representative transverse sections at a rostral (A) and caudal (B) telencephalic level illustrate the relative position of striatal and pallidal structures.
• Although in the literature different names have been given to homologous structures, the same colours have been used for comparable regions in each tetrapod to simplify identification.
*** See paper for abbreviations ***

5

Basal ganglia modulate motor outputs and action selection (Smeets et al., 2000) research

Jia et al. (2010)

6

Jia et al. (2010)

The role of electro-acupuncture (EA) stimulation on motor symptoms in Parkinson's disease (PD) has not been well studied. In a rat hemiparkinsonian model induced by unilateral transection of the medial forebrain bundle (MFB). EA stimulation improved motor impairment in a frequency-dependent manner. Whereas EA stimulation at a low frequency (2 Hz) had no effect, EA stimulation at a high frequency (100 Hz) significantly improved motor coordination. However, neither low nor high EA stimulation could significantly enhance dopamine levels in the striatum. EA stimulation at 100 Hz normalized the MFB lesion-induced increase in midbrain GABA content, but it had no effect on GABA content in the globus pallidus. These results suggest that high-frequency EA stimulation improves motor impairment in MFB-lesioned rats by increasing GABAergic inhibition in the output structure of the basal ganglia.

7

Basal ganglia already appear in the early vertebrates (Stephenson-Jones et al., 2011)

• All of major components of basal ganglia in phylogenetically oldest group of vertebrates, lampreys (jawless fish)
• Exaptation: function changed to perf similar computations for diff info in parallel loops (functional modules) - motor, emotional and cog
• Limbic module: pref for reward (e.g. Lobo et al., 2010)
• Motor module: action selection (e.g. Kravitz et al., 2010)
- Multiply basal ganglia connections

see notes

8

Basal ganglia already appear in the early vertebrates (Stephenson-Jones et al., 2011) research

• Background
○ Although the basal ganglia are thought to play a key role in action selection in mammals, it is unknown whether this mammalian circuitry is present in lower vertebrates as a conserved selection mechanism. We aim here, using lamprey, to elucidate the basal ganglia circuitry in the phylogenetically oldest group of vertebrates (cyclostomes) and determine how this selection architecture evolved to accommodate the increased behavioral repertoires of advanced vertebrates.
• Results
○ We show, using immunohistochemistry, tract tracing, and whole-cell recordings, that all parts of the mammalian basal ganglia (striatum, globus pallidus interna [GPi] and externa [GPe], and subthalamic nucleus [STN]) are present in the lamprey forebrain. In addition, the circuit features, molecular markers, and physiological activity patterns are conserved. Thus, GABAergic striatal neurons expressing substance P project directly to the pallidal output layer, whereas enkephalin-expressing striatal neurons project indirectly via nuclei homologous to the GPe and STN. Moreover, pallidal output neurons tonically inhibit tectum, mesencephalic, and diencephalic motor regions.
• Conclusions
- These results show that the detailed basal ganglia circuitry is present in the phylogenetically oldest vertebrates and has been conserved, most likely as a mechanism for action selection used by all vertebrates, for over 560 million years. Our data also suggest that the mammalian basal ganglia evolved through a process of exaptation, where the ancestral core unit has been co-opted for multiple functions, allowing them to process cognitive, emotional, and motor information in parallel and control a broader range of behaviors.

9

Of flies and men: arthropod central complex homologous to BG? (Strausfeld & Hirth, 2013; Fiore et al., 2015)

• Similarities in action selection circuitries
• Sensorimotor loop responsible for processing multiple sensory stim that are somatotopically (mapped relative to body) organised
- Modulated by dopamine amplifying info and mediating learning

see notes

10

Fiore et al. (2015)

Survival and reproduction entail the selection of adaptive behavioural repertoires. This selection manifests as phylogenetically acquired activities that depend on evolved nervous system circuitries. Lorenz and Tinbergen already postulated that heritable behaviours and their reliable performance are specified by genetically determined programs. Here we compare the functional anatomy of the insect central complex and vertebrate basal ganglia to illustrate their role in mediating selection and maintenance of adaptive behaviours. Comparative analyses reveal that central complex and basal ganglia circuitries share comparable lineage relationships within clusters of functionally integrated neurons. These clusters are specified by genetic mechanisms that link birth time and order to their neuronal identities and functions. Their subsequent connections and associated functions are characterized by similar mechanisms that implement dimensionality reduction and transition through attractor states, whereby spatially organized parallel-projecting loops integrate and convey sensorimotor representations that select and maintain behavioural activity. In both taxa, these neural systems are modulated by dopamine signalling that also mediates memory-like processes. The multiplicity of similarities between central complex and basal ganglia suggests evolutionarily conserved computational mechanisms for action selection. We speculate that these may have originated from ancestral ground pattern circuitries present in the brain of the last common ancestor of insects and vertebrates.

11

Injection of APV impairs reward-based action learning (Yin et al., 2005)

• 2 learning processes in dorsal striatum
○ Sensorimotor that mediates stim-dependent habitual responses (dorsolateral striatum)
○ Associate required for learning goal-directed actions (dorsomedial striatum)
• Operant conditioning
○ Pretraining: rats trained to perf 2 lever-press actions for common outcome
○ Training: single session during which 2 actions rewarded with unique outcomes (encode unique action-outcome associations); food pellets and fruit punch
○ Test: outcome devaluation test (satiate with reward prior to test), discrim between lever predicting devalued (Dev) and non-devalued (Non) reward
• Infusion of APV (aCSF - artificial cerebral spinal fluid in controls):
- Effective after pretraining
- Not effective after training

see notes

12

Injection of APV impairs reward-based action learning (Yin et al., 2005) research

Although there is consensus that instrumental conditioning depends on the encoding of action–outcome associations, it is not known where this learning process is localized in the brain. Recent research suggests that the posterior dorsomedial striatum (pDMS) may be the critical locus of these associations. We tested this hypothesis by examining the contribution of N‐methyl‐d‐aspartate receptors (NMDARs) in the pDMS to action–outcome learning. Rats with bilateral cannulae in the pDMS were first trained to perform two actions (left and right lever presses), for sucrose solution. After the pre‐training phase, they were given an infusion of the NMDA antagonist 2‐amino‐5‐phosphonopentanoic acid (APV, 1 mg/mL) or artificial cerebral spinal fluid (ACSF) before a 30‐min session in which pressing one lever delivered food pellets and pressing the other delivered fruit punch. Learning during this session was tested the next day by sating the animals on either the pellets or fruit punch before assessing their performance on the two levers in extinction. The ACSF group selectively reduced responding on the lever that, in training, had earned the now devalued outcome, whereas the APV group did not. Experiment 2 replicated the effect of APV during the critical training session but found no effect of APV given after acquisition and before test. Furthermore, Experiment 3 showed that the effect of APV on instrumental learning was restricted to the pDMS; infusion into the dorsolateral striatum did not prevent learning. These experiments provide the first direct evidence that, in instrumental conditioning, NMDARs in the dorsomedial striatum are involved in encoding action–outcome associations

13

Basal ganglia are involved in motor learning (Doyon & Benali, 2005)

Experience-dependent changes in the brain depend on whether subjects are required to learn a new sequence of movements (motor sequence learning)/learn to adapt to env perturbations (motor adaptation)

see notes

14

Basal ganglia are involved in motor learning (Doyon & Benali, 2005) research

Sato et al. (2020)

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Sato et al. (2020)

Motor skill learning leads to task-related contextual behavioral changes that are underpinned by neuroplastic cortical reorganization. Short-term training induces environment-related contextual behavioral changes and neuroplastic changes in the primary motor cortex (M1). However, it is unclear whether environment-related contextual behavioral changes persist after long-term training and how cortical plastic changes are involved in behavior. To address these issues, we examined 14 elite competitive swimmers and 14 novices. We hypothesized that the sensorimotor skills of swimmers would be higher in a water environment than those of novices, and the recruitment of corticospinal and intracortical projections would be different between swimmers and novices. We assessed joint angle modulation performance as a behavioral measure and motor cortical excitation and inhibition using transcranial magnetic stimulation (TMS) at rest and during the tasks that were performed before, during, and after water immersion (WI). Motor cortical inhibition was measured with short-interval intracortical inhibition and long-interval intracortical inhibition by a paired-pulse TMS paradigm. We found that 1) the sensorimotor skills of swimmers who underwent long-term training in a water environment were superior and robustly unchanged compared with those of novices with respect to baseline on land, during WI, on land post-WI and 2) intracortical inhibition in water environments was increased in swimmers but was decreased in non-swimmers at rest compared to that on land; however, the latter alterations in intracortical inhibition in water environment were insufficient to account for the superior sensorimotor skills of swimmers. In conclusion, we demonstrate that environment-related contextual behavioral and neural changes occur even with long-term training experience.

16

Sensory mapping can change with perceptual experience and learning (Rasumssen, 1982; Merzenich et al., 1984; Recanzone et al., 1990; Pleger et al., 2003; Gunduz et al., 2020)

• Cortical representations can change with use: owl monkey train for several months at task using fingers 2-4
• Reorganisation of somatosensory cortex maps following:
○ Digit amputations in racoon and monkey
○ Peripheral nerve stim in cats
Passive touching of fingertips in humans (fMRI, primary and second somatosensory cortex)

see notes

17

Sensory mapping can change with perceptual experience and learning (Rasumssen, 1982; Merzenich et al., 1984; Recanzone et al., 1990; Pleger et al., 2003; Gunduz et al., 2020) research

Elbert et al. (1995)

Huxlin et al. (2009)

Orban et al. (2004)

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Elbert et al. (1995)

see notes

• Areas in somatosensory cortex changed - distance between digit 1-5 in brain map
- And the same thing happens I humans after being trained for specific task

19

Huxlin et al. (2009)

Damage to the adult, primary visual cortex (V1) causes severe visual impairment that was previously thought to be permanent, yet several visual pathways survive V1 damage, mediating residual, often unconscious functions known as “blindsight.” Because some of these pathways normally mediate complex visual motion perception, we asked whether specific training in the blind field could improve not just simple but also complex visual motion discriminations in humans with long-standing V1 damage. Global direction discrimination training was administered to the blind field of five adults with unilateral cortical blindness. Training returned direction integration thresholds to normal at the trained locations. Although retinotopically localized to trained locations, training effects transferred to multiple stimulus and task conditions, improving the detection of luminance increments, contrast sensitivity for drifting gratings, and the extraction of motion signal from noise. Thus, perceptual relearning of complex visual motion processing is possible without an intact V1 but only when specific training is administered in the blind field. These findings indicate a much greater capacity for adult visual plasticity after V1 damage than previously thought. Most likely, basic mechanisms of visual learning must operate quite effectively in extrastriate visual cortex, providing new hope and direction for the development of principled rehabilitation strategies to treat visual deficits resulting from permanent visual cortical damage.

20

Orban et al. (2004)

The advent of functional magnetic resonance imaging (fMRI) in non-human primates has facilitated comparison of the neurobiology of cognitive functions in humans and macaque monkeys, the most intensively studied animal model for higher brain functions. Most of these comparative studies have been performed in the visual system. The early visual areas V1, V2 and V3, as well as the motion area MT are conserved in humans. Beyond these areas, differences between human and monkey functional organization are increasingly evident. At the regional level, the monkey inferotemporal and intraparietal complexes appear to be conserved in humans, but there are profound functional differences in the intraparietal cortex suggesting that not all its constituent areas are homologous. In the long term, fMRI offers opportunities to compare the functional anatomy of a variety of cognitive functions in the two species.

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Plasticity in sensory and motor systems is reciprocally linked (Ostry & Gribble, 2016)

• Acquisition of motor skills involves both perceptual and motor learning
• Playing tennis - learning to feel a good serve - learned perception
• Learning a language - learning to distinguish its sounds
• Combining passive movement with sensory input (follow direction of movement) improves learning of complex trajectories (Wong et al., 2012)
- Changes in connectivity that strengthens networks in both primary motor cortex (M1) and primary somatosensory cortex (S1)

see notes

Changes in motor and somatosensory cortex even though motor task in principle

22

Plasticity in sensory and motor systems is reciprocally linked (Ostry & Gribble, 2016) research

Lee and Whitt (2015)

Barkan et al. (2017)

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Lee and Whitt (2015)

Sensory loss leads to widespread adaptation of brain circuits to allow an organism to navigate its environment with its remaining senses, which is broadly referred to as cross-modal plasticity. Such adaptation can be observed even in the primary sensory cortices, and falls into two distinct categories: recruitment of the deprived sensory cortex for processing the remaining senses, which we term ‘cross-modal recruitment’, and experience-dependent refinement of the spared sensory cortices referred to as ‘compensatory plasticity.’ Here we will review recent studies demonstrating that cortical adaptation to sensory loss involves LTP/LTD and homeostatic synaptic plasticity. Cross-modal synaptic plasticity is observed in adults, hence cross-modal sensory deprivation may be an effective way to promote plasticity in adult primary sensory cortices.

24

Barkan et al. (2017)

Studies in Passerines have found that migrating species recruit more new neurons into brain regions that process spatial information, compared with resident species. This was explained by the greater exposure of migrants to spatial information, indicating that this phenomenon enables enhanced navigational abilities. The aim of the current study was to test this hypothesis in another order—the Columbiformes – using two closely-related dove species—the migrant turtle-dove (Streptopelia turtur) and the resident laughing dove (S. senegalensis), during spring, summer, and autumn. Wild birds were caught, treated with BrdU, and sacrificed 5 weeks later. New neurons were recorded in the hyperpallium apicale, hippocampus and nidopallium caudolaterale regions. We found that in doves, unlike passerines, neuronal recruitment was lower in brains of the migratory species compared with the resident one. This might be due to the high sociality of doves, which forage and migrate in flocks, and therefore can rely on communal spatial knowledge that might enable a reduction in individual navigation efforts. This, in turn, might enable reduced levels of neuronal recruitment. Additionally, we found that unlike in passerines, seasonality does not affect neuronal recruitment in doves. This might be due to their non-territorial and explorative behavior, which exposes them to substantial spatial information all year round. Finally, we discuss the differences in neuronal recruitment between Columbiformes and Passeriformes and their possible evolutionary explanations. Our study emphasizes the need to further investigate this phenomenon in other avian orders and in additional species.

25

Vision supplements hearing in owl prey detection (De Bello et al., 2001)

• Auditory map in external nucleus of midbrain aligned with retinotopic visual input and controls head movements (via hindbrain)
• During devel experimental manips targeted auditory input (ear plug) and visual input (prism) - when removed, sound-guided gaze movements displaced (but not visual gaze) - effect strong in owls <3 weeks (critical period)
- During critical period owls can learn better and correct larger misalignments than later

see notes

26

Vision supplements hearing in owl prey detection (De Bello et al., 2001) research

Friedel et al. (2020)

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Friedel et al. (2020)

Are alternation and co-occurrence of stimuli of different sensory modalities conspicuous? In a novel audio-visual oddball paradigm, the P300 was used as an index of the allocation of attention to investigate stimulus- and task-related interactions between modalities. Specifically, we assessed effects of modality alternation and the salience of conjunct oddball stimuli that were defined by the co-occurrence of both modalities. We presented (a) crossmodal audio-visual oddball sequences, where both oddballs and standards were unimodal, but of a different modality (i.e., visual oddball with auditory standard, or vice versa), and (b) oddball sequences where standards were randomly of either modality while the oddballs were a combination of both modalities (conjunct stimuli). Subjects were instructed to attend to one of the modalities (whether part of a conjunct stimulus or not). In addition, we also tested specific attention to the conjunct stimuli. P300-like responses occurred even when the oddball was of the unattended modality. The pattern of event-related potential (ERP) responses obtained with the two crossmodal oddball sequences switched symmetrically between stimulus modalities when the task modality was switched. Conjunct oddballs elicited no oddball response if only one modality was attended. However, when conjunctness was specifically attended, an oddball response was obtained. Crossmodal oddballs capture sufficient attention even when not attended. Conjunct oddballs, however, are not sufficiently salient to attract attention when the task is unimodal. Even when specifically attended, the processing of conjunctness appears to involve additional steps that delay the oddball response.

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Development of the visual system in mammals after birth

• Diffs in visual abilities of adults and infants
○ Acuity develops during first year v. fast but continues also during later development (up to age 20) as the eye (and lens) continues growing in size
○ In the first month eye-hand coord already starts developing
○ By week 8, babies more easily focus view
○ By 3 months reaching for objects
○ Crawling (approx. 8 months) develops eye-foot-hand coord further
○ Ny 10 months increased visual generalisation for small features in non-relevant objects and improved human face discrim (relevant objects)
- Have poor resolution when born

see notes

29

Development of the visual system in mammals after birth research

Gilbert and Walsh (2004)

30

Gilbert and Walsh (2004)

The primary visual cortex is, of course, for vision – or so you would think. But it seems that, in blind people, the primary visual cortex can take on an important role in language processing. This suggests considerable flexibility in the processes by which subregions of the human brain become specialised for different functions