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First published online May 18, 2006
Journal of Experimental Biology 209, 2015-2024 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02240

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Activation of a sensorimotor pathway in response to a water temperature drop in a teleost fish

E. H. van den Burg^1,*, M. Verhoye², R. R. Peeters², J. Meek¹, G. Flik¹ and A. Van der Linden²

¹ Department of Organismal Animal Physiology, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands
² Bio-Imaging Lab, Campus Groenenborger, University of Antwerp, Antwerp, Belgium

View larger version (37K): [in a new window]   Fig. 1. Partial brain atlas of common carp. Horizontal sections of 10 µm were stained according to Kluver-Barrera. Horizontal distance between consecutive sections is 1 mm. Section A is the most ventral, and the bar on the left of the sections indicates corresponding sectioning of the magnetic resonance images shown in Fig. 2. The scale bar is 2 mm. See List for abbreviations.

View larger version (101K): [in a new window]   Fig. 2. Identification of brain structures in magnetic resonance images (MRI). (A) Lateral reconstruction of a carp brain, on the basis of transversal sections. (B) Lateral reconstruction with lines that indicate the middle of the acquired adjacent 1 mm fMRI slices through the carp brain. The number of each line corresponds to the image number C. (C) T2-weighted high resolution spin echo images of horizontal 1 mm slices through the carp brain. Scale bar, 5 mm. See List for abbreviations.

View larger version (55K): [in a new window]   Fig. 3. Activation at the nerve entrance (N) following a 10°C temperature drop, as determined by blood oxygenation level-dependent-weighted (BOLD) functional magnetic resonance images (fMRI). (A) T2-weighted high-resolution spin echo image showing the complex (N) of trigeminal, facial, acoustic and anterior lateral line nerve extending from the brain. The image resolution does not allow for separate identification of the cranial nerves. tel, telencephalon. (B) Average of the color-coded percentual BOLD difference maps within the first 5 min after the onset of the temperature drop overlaid on the high-resolution image. The brain region surrounding the entrance of the cranial nerves is transiently activated (blue, reduced BOLD signal intensities). Some increase in BOLD signal intensities (red) can sometimes be observed in other brain regions. Scale bar, 2.5 mm. (C) The transient decrease of BOLD signal intensity measured in the region surrounding the entrance of the cranial nerves is not accompanied by any substantial change in cerebral blood volume (CBV; D) from which it is concluded that the decreased BOLD signal is a result of increased cellular activity. (D) CBV signal intensity changes in the region surrounding the entrance of the cranial nerves. Values are means ± s.d. (N=3).

View larger version (63K): [in a new window]   Fig. 4. Anatomy of the region where the cranial nerves extend from the brain. (A) Horizontal section, stained according to Kluver-Barrera. The orange line surrounds the region of activation. (B) Drawing of the section shown in A delineating the sensory root of the trigeminal nerve (Vs) and other areas and nerves. The V is located rostrally to the facial nerve (VIIs) and the anterior lateral line nerve (alln). It projects to the trigeminal motor nucleus (NVmd) that innervates the muscles of the jaws. (C) Transverse section in the region of the sensory and motor nuclei associated with the trigeminal nerve. (D) Drawing of the section shown in C, delineating the location of the primary sensory trigeminal nucleus (NVs) dorsally to the trigeminal motor nuclei (NVmd and NVmv), and ventrally to the commissure of the secondary gustatory nuclei (cgus). The NVs receives input from the trigeminal nerve and projects to the valvula cerebelli. For other abbreviations, see List of abbreviations. Scale bar, 0.3 mm (A,B) and 0.2 mm (C,D).

View larger version (49K): [in a new window]   Fig. 5. Activation of the valvula cerebelli following a 10°C temperature drop as determined by blood oxygenation level-dependent (BOLD)-weighted and cerebral blood volume (CBV)-weighted functional magnetic resonance images (fMRI). (A) T2-weighted high-resolution spin echo image showing the location of the corpus cerebelli (cc), the valvula cerebelli (vc), and the tectum opticum (to). (B) Average of the color-coded percentual BOLD difference maps within the first 5 min after the onset of the temperature drop overlaid on the high-resolution image. The valvula cerebelli, but not the tectum opticum shows a reduced BOLD signal intensity (blue). This fish (but not the other two examined) also demonstrated pronounced early BOLD signal increase (red) in the corpus cerebellum. (C) Biphasic change of BOLD signal intensity measured in the valvula cerebelli indicates activation followed by inactivation of this brain region following the temperature drop. (D) Transient decrease of CBV signal reveals increased blood supply to the valvula cerebelli, demonstrating that the decrease of the BOLD signal is caused by increased cellular activity. Scale bar, 2.5 mm (A,B). Values are means ± s.d. (N=3).

View larger version (21K): [in a new window]   Fig. 6. Schematic representation of the adaptive and sensorimotor pathway as derived from our fMRI studies (this study) (Van den Burg et al., 2005), and from several neuroanatomical studies. The acclimation pathway is probably triggered by a reduction of the temperature of the cerebral blood, and starts with thermodetection in the preoptic area (poa), where also a subsequent stress response is initiated. This leads to activation of the pituitary pars distalis (pd; to stimulate the release of ACTH). The sensorimotor pathway is probably triggered by trigeminal cold-receptors in the buccal cavity, and involves sequential activation of the sensory root of the trigeminal nerve (N), the associated sensory nucleus (NVs) and the valvula cerebelli (vc). The vc probably stimulates one or more motor nuclei (the nucleus of the medial longitudinal fascicle (nmlf), the nucleus ruber (nr) and the reticular formation (srf and imrf) to initiate (broken lines) swimming behavior.