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Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats

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Abstract

Learning can be categorized into cue-instructed and spontaneous learning types; however, so far, there is no detailed comparative analysis of specific brain pathways involved in these learning types. The aim of this study was to compare brain activity patterns during these learning tasks using the in vivo imaging technique of single photon-emission computed tomography (SPECT) of regional cerebral blood flow (rCBF). During spontaneous exploratory learning, higher levels of rCBF compared to cue-instructed learning were observed in motor control regions, including specific subregions of the motor cortex and the striatum, as well as in regions of sensory pathways including olfactory, somatosensory, and visual modalities. In addition, elevated activity was found in limbic areas, including specific subregions of the hippocampal formation, the amygdala, and the insula. The main difference between the two learning paradigms analyzed in this study was the higher rCBF observed in prefrontal cortical regions during cue-instructed learning when compared to spontaneous learning. Higher rCBF during cue-instructed learning was also observed in the anterior insular cortex and in limbic areas, including the ectorhinal and entorhinal cortexes, subregions of the hippocampus, subnuclei of the amygdala, and the septum. Many of the rCBF changes showed hemispheric lateralization. Taken together, our study is the first to compare partly lateralized brain activity patterns during two different types of learning.

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Abbreviations

Acb:

Nucleus accumbens

Acbsh:

n. accumbens—shell region

Acbc:

n. accumbens—core region

AH:

Anterior hypothalamus

Au1:

Primary auditory cortex

Au2:

Secondary auditory cortex

BA:

Anterior basal amygdala

BNST:

Bed nucleus of the stria terminalis

BP:

Posterior basal amygdala

CeA:

Central amygdala

Cg1:

Cingular cortex

CoA:

Cortical amygdala

CoM:

Corpus mammillare

CPu:

Caudate putamen

Ect:

Ectorhinal cortex

Ent:

Entorhinal cortex

GP:

Globus pallidus

Hip:

Hippocampus

IC:

Inferior colliculus

IL:

Infralimbic cortex

aIn:

Anterior insular cortex

pIn:

Posterior insular cortex

IP:

Interpeduncular nucleus

LA:

Lateral amygdala

LG:

Lateral geniculatum

LH:

Lateral hypothalamus

LS:

Lateral septum

M1:

Primary motor cortex

M2:

Secondary motor cortex

MeA:

Medial amygdala

MG:

Medial geniculatum

MH:

Medial hypothalamus

MO:

Medial orbitofrontal cortex

MS:

Medial septum

ON:

Olfactory nucleus

OT:

Olfactory tubercle

PAG:

Periaqueductal gray

Pir:

Piriform cortex

Pn:

Pontine nucleus

PRh:

Perirhinal cortex

PrL:

Prelimbic cortex

PTA:

Area pretectalis

PtA:

Parietal association cortex

RNc:

Raphe nuclei

RSA:

Agranular retrosplenial cortex

RSG:

Granular retrosplenial cortex

S1BF:

Primary somatosensory cortex—barrel cortex

S1FL:

Primary somatosensory cortex—forelimbs

S1HL:

Primary somatosensory cortex—hindlimbs

S1J:

Primary somatosensory cortex—jaw region

S1ULp:

Primary somatosensory cortex—upper lip

S2:

Secondary somatosensory cortex

SC:

Superior colliculus

SF:

Septofimbrial nucleus

SG:

Subgeniculatum

SN:

Substantia nigra

Sub:

Subiculum

TeA:

Temporal association cortex

Tg:

Tegmentum

Th:

Thalamus

TS:

Triangular septum

TT:

Taenia tecta

V1B:

Primary visual cortex—binocular area

V1M:

Primary visual cortex—monocular area

V2L:

Secondary visual cortex—lateral

V2M:

Secondary visual cortex—medial

VG:

Ventral geniculatum

VO/LO:

Ventral/lateral orbitofrontal cortex

VP:

Ventral pallidum

VTA:

Ventral tegmental area

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Acknowledgements

We thank Madeleine Stiefel for help with editorial work. This work was supported by the Bundesministerium für Bildung und Forschung, Grant No: 01KR1304B (TRANSGEN) to K.B. and Grant No: 01KR1207D (UBICA) to J.B.

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Correspondence to Katharina Braun.

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Mannewitz, A., Bock, J., Kreitz, S. et al. Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats. Brain Struct Funct 223, 2025–2038 (2018). https://doi.org/10.1007/s00429-017-1605-x

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  • DOI: https://doi.org/10.1007/s00429-017-1605-x

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