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Neuroplastic Changes in the Superior Colliculus and Hippocampus in Self-rewarding Paradigm: Importance of Visual Cues

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Abstract

Coincident excitation via different sensory modalities encoding objects of positive salience is known to facilitate learning and memory. With a view to dissect the contribution of visual cues in inducing adaptive neural changes, we monitored the lever press activity of a rat conditioned to self-administer sweet food pellets in the presence/absence of light cues. Application of light cues facilitated learning and consolidation of long-term memory. The superior colliculus (SC) of rats trained on light cue showed increased neuronal activity, dendritic branching, and brain-derived neurotrophic factor (BDNF) protein and mRNA expression. Concomitantly, the hippocampus showed augmented neurogenesis as well as BDNF protein and mRNA expression. While intra-SC administration of U0126 (inhibitor of ERK 1/2 and long-term memory) impaired memory formation, lidocaine (local anaesthetic) hindered memory recall. The light cue–dependent sweet food pellet self-administration was coupled with increased efflux of dopamine (DA) and 3,4-dihydroxyphenylacetic acid (DOPAC) in the nucleus accumbens shell (AcbSh). In conditioned rats, pharmacological inhibition of glutamatergic signalling in dentate gyrus (DG) reduced lever press activity, as well as DA and DOPAC secretion in the AcbSh. We suggest that the neuroplastic changes in the SC and hippocampus might represent memory engrams sculpted by visual cues encoding reward information.

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taken from the demarcated area (not to scale) in s and t (coordinates, bregma − 2.56 mm) (Paxinos and Watson, 1998). c, f, i, l, o and r show co-labeled cells with BrdU and NeuN antibodies and the insets (c’, f’, i’, l’, o’ and r’) show co-labeled cells at higher magnification respectively. The morphometric data were analysed using a one-way ANOVA followed by post hoc Bonferroni’s multiple comparison test and represented as mean ± SEM (n = 5/group) and power > 0.9. *p < 0.001 versus no reward + no light cue control; #p < 0.01, ##p < 0.001 versus no light cue control. Scale bar = 100 μm (a–r), and 25 μm (all insets). D3V, dorsal third ventricle; DG, dentate gyrus; str. or, stratum oriens; str. pyr, stratum pyramidale; str. rad, stratum radiatum

Fig. 8

taken from the demarcated area (not to scale) in s and t (coordinates, bregma − 2.56 mm) (Paxinos and Watson, 1998). c, f, i, l, o and r show cells co-labeled with BrdU and NeuN antibodies, and the insets (c’, f’, i’, l’, o’ and r’) show co-labeled cells at higher magnification respectively. The morphometric data were analysed using a one-way ANOVA followed by post hoc Bonferroni’s multiple comparison test and represented as mean ± SEM (n = 5/group) and power > 0.9. *p < 0.001 versus no reward + no light cue control; #p < 0.001 versus no light cue control. Scale bar = 100 μm (a–r) and 25 μm (all insets). D3V, dorsal third ventricle; GCL, granule cell layer; ML, molecular layer; str. or, stratum oriens; str. pyr, stratum pyramidale; str. rad, stratum radiatum; SGZ, subgranular zone

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Abbreviations

Acb:

Nucleus accumbens

AcbSh:

Nucleus accumbens shell

aCSF:

Artificial cerebrospinal fluid

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

AP:

Anterior posterior

AUC:

Area under the curve

BDNF:

Brain-derived neurotrophic factor

BrdU:

5-bromo-2-deoxyuridine

CREB:

cAMP response element-binding protein

DA:

Dopamine

DAB:

3,3′-Diaminobenzidine tetrahydrochloride

DG:

Dentate gyrus

DOPAC:

3,4-Dihydroxyphenylacetic acid

DpG:

Deep grey layer

DpWh:

Deep white layer

DV:

Dorsal ventral

Elk-1:

Erythroblast transformation specific like-1

ERK:

Extracellular signal-regulated kinase

FR1:

Fixed ratio 1

HPLC-ECD:

High-performance liquid chromatography with electrochemical detector

HRP:

Horseradish peroxidase

InG:

Intermediate grey layer

InWh:

Intermediate white layer

NMDA:

N-methyl-D-aspartic acid

ip:

Intraperitoneal

LTP:

Long-term potentiation

MEK:

Mitogen-activated protein kinase

ML:

Medial lateral

NeuN:

Neuronal nuclear protein

Op:

Optic layer

PBS:

Phosphate-buffered saline

PMSF:

Phenylmethylsulfonyl fluoride

qRT-PCR:

Quantitative reverse transcription polymerase chain reaction

RIPA:

Radioimmuno-precipitation assay

RT:

Retention time

SC:

Superior colliculus

SDS:

Sodium dodecyl sulphate

SuG:

Superficial grey layer

VTA:

Ventral tegmental area

Zo:

Zonal layer

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Acknowledgements

SNA acknowledges the Indian Council of Medical Research (ICMR) for providing senior research fellowship (45/06/2020/PHA/BMS).This work was supported by grants from the Science and Engineering Research Board (SERB) (CRG/2020/004971), Govt. of India, New Delhi, India.AJS acknowledges the funds received from SERB (GOI; EMR/2017/000621) and Council for Scientific and Industrial Research [(CSIR), GOI (37[1718]/18/EMR-II)]. We thank Yash Bhatt, 6025 Falling View Lane, Cumming, GA 30040, USA, for critical reading of the manuscript.

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Authors and Affiliations

  1. Department of Pharmaceutical Sciences, Rashtrasant Tukadoji Maharaj Nagpur University, Nagpur, 440 033, India

    Sanjay N. Awathale, Akash M. Waghade, Harish M. Kawade & Dadasaheb M. Kokare

  2. Department of Biotechnology, Savitribai Phule Pune University, Pune, 411 007, India

    Gouri Jadhav & Amul J. Sakharkar

  3. Indian Institute of Science Education and Research (IISER), Dr. Homi Bhabha Road, Pune, 411 008, India

    Amit G. Choudhary & Nishikant K. Subhedar

  4. Department of Zoology, Savitribai Phule Pune University, Pune, 411 007, India

    Sneha Sagarkar

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  1. Sanjay N. Awathale
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Contributions

Study conception and design, NKS, DMK, and SNA; behavioural, biochemical, and IHC data collection, SNA and AMW; protein and mRNA data collection, HMK, GJ, SS, and AJS; analysis and interpretation of results, SNA, AGC, NKS, AJS, and DMK; draft manuscript preparation, NKS, SNA, AGC, and DMK. All authors reviewed the results and approved the final version of the manuscript.

Corresponding author

Correspondence to Dadasaheb M. Kokare.

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Protocols employed in the present study were carried out in accordance with the Institutional Animal Ethics Committee, Department of Pharmaceutical Sciences, Rashtrasant Tukadoji Maharaj Nagpur University, Nagpur, India.

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Awathale, S.N., Waghade, A.M., Kawade, H.M. et al. Neuroplastic Changes in the Superior Colliculus and Hippocampus in Self-rewarding Paradigm: Importance of Visual Cues. Mol Neurobiol 59, 890–915 (2022). https://doi.org/10.1007/s12035-021-02597-2

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