Is there a morphine store in the brain of the camel?



Is there a morphine store in the brain of the camel?

by Laurence Garey and Eric Mensah-Brown
Department of Anatomy
Faculty of Medicine and Health Sciences
UAE University
PO Box 17666
Al Ain, United Arab Emirates

Summary

As part of the camel brain project supported by the Al Ain Chapter of ENHG, we have studied the superior colliculus, a region on the surface of the brainstem of the camel, Camelus dromedarius, using modern immunohistochemical techniques. We had observed that, unlike in most mammals, the superior colliculus of the camel is much larger than the inferior colliculus, another similar nervous centre lying alongside it. It is known that the superior colliculus is concerned with visual reflexes and head, neck and eye movements, of obvious importance to this animal with large eyes, head and neck, and apparent good vision. We looked at the distribution of neuropeptides, chemicals that help the transmission of information around the brain. We describe for the first time an unusually large content of neurons in the superior colliculus that contain enkephalin, an opioid (morphine-like substance). We propose that this system is associated with a pain-inhibiting pathway in the brain and spinal cord that could be important in relation to the camel's life in the harsh environment of its native deserts.

Introduction

The mammalian brain consists essentially of the cerebral hemispheres, covered by the cerebral cortex, the cerebellum related largely to motor integration and learning, and the brainstem which links the hemispheres to the spinal cord. Whereas the hemispheres and cortex are the prime location for sensory integration and motor activity, together with higher cognitive function, the brainstem (medulla, pons and midbrain) contains neural centres that support reflex activity. The superior and inferior colliculi form laminated eminences on the dorsal surface of the midbrain. The superior colliculi are related to visual reflexes, whereas the inferior colliculi form part of the auditory pathway.

Many studies have established the architecture of the colliculi in species from rodents to man. However a perusal of the literature reveals a paucity of information on large mammals, such as the camel. The camel is held in local folklore to possess exceptional visual capabilities, a quality that has aided its adaptation to the arid environment of the desert (Figure 1).

Results

We obtained the brains of adult male camels aged between 2 and 4 years from a commercial abattoir. After standard laboratory preparation, we examined sections of the colliculus with a microscope. We also made observations on skulls collect from the local desert, and a brain kindly made available by Drs U Wernery and J Kinne.

The cranial cavity of the camel is small compared with the whole skull (Figure 2). Its brain is also relatively small, up to about 500g (Figure 3), considering its large total body mass. We were surprised to find that its superior colliculus was several times the volume of the inferior colliculus (Figure 3), whereas as in most species (including man) the two are approximately the same size (Figure 4). . This difference in size could be significant because the dolphin, an ungulate like the camel, is known to have an elaborate auditory system and possesses an inferior colliculus that is much larger than the superior colliculus (Figure 5). So, the main aim of our study was to determine to what extent the very large superior colliculus of the camel might have a special neuronal architecture or distribution of neurotransmitters that are responsible for passage of neural information between nerve cells.

The superior colliculus is composed of layers of alternating grey matter (largely composed of neuronal cell bodies) and white matter (containing mainly nerve fibres) (Figure 6). The superficial layers receive nerve fibres (axons) from the retina of the eye (Figure 7) and from the visual cortex, the highest processing area for visual information coming from the retina. The superior colliculus is also involved in processing sensory information from other modalities than just visual, including feedback to its deeper layers from the auditory, general sensory and motor regions of the cerebral cortex. This is consistent with the superior colliculus being an important centre for the control of orientation of head and eye.

We found that the neuronal architecture of the superior colliculus of the camel is similar to that of other mammals. Neuronal cell bodies containing certain common neuropeptides are limited to the superficial layers (Figure 8), whereas others are restricted to deeper layers, and yet others are only in the grey matter deep to the superior colliculus, the so-called periaqueductal grey (PAG).

Of the peptides we studied, the most interesting were the enkephalins (or endorphins). These "intrinsic opioids" are important in the regulation of pain. In particular, met-enkephalin neurons showed striking differences from what has been described before. Most were small, and predominantly in the superficial layers, but some larger met-enkephalin neurons were observed, especially in the intermediate grey layer ( (Figure 9), (Figure 10)). Long enkephalin fibres were observed bridging between the superficial, intermediate and deep layers, while some extended into the PAG (Figure 11).

Discussion

The very large size of the superior colliculus of the camel brain suggests it may have a special function in this animal. This may be related to a well-developed visual system, and the necessity for the camel to coordinate eye and head and movements accentuated by its long, muscular neck. However, our discovery of numerous large met-enkephalin neurons in the superior colliculus suggests a specialisation of this part of the brain compared with other mammals studied so far.

Previously, enkephalins in the superior colliculus have been described mainly in a minor population of small neurons in the superficial layers. We confirm this presence of small enkephalin neurons in the superficial, visual layers. However, in the camel a considerable population of large enkephalin neurons is found in the deep layers. Enkephalins are important in pain suppression in central neural pathways: they are endogenous opiates. They may explain the well-known phenomenon of initial inhibition of pain sensation that can last for several hours after an injury. A pain inhibitory pathway (Figure 12) has been described from the PAG to the lower brainstem, and thence to the spinal cord. We propose that the presence of numerous large enkephalin neurons throughout the superior colliculus with fibres projecting to the PAG suggests that the pain inhibiting opioid pathway may be especially well developed in the camel, perhaps helping to suit it for the extremes of temperature and discomfort one might expect it to suffer in the desert.

Acknowledgements

This work was supported by grants from the UAE University and the Emirates Natural History Group, Al Ain. We thank Ulrich Wernery and Joerg Kinne for help with initial pilot experiments. Our special thanks are due to the late Alyaa Ali Hussain Talib without whose devotion these observations would never have been made.

Figures



Figure 1. The camel in typical desert surroundings. There is little protection from the sun at any time of the day.



Figure 2. The skull of the camel has rather little space for the brain (between the arrows).



Figure 3. The camel brain is like most ungulate brains and only weighs about 500g in spite of the large body mass. The very large superior colliculus (arrow) is obvious (specimen with grateful thanks to U Wernery and J Kinne).



Figure 4. Medial view of the human brain. Note that the colliculi (arrowed) are about the same size.



Figure 5. In the dolphin, the inferior colliculus (IC) is much larger than the superior (SC). This may be related to the important auditory functions of this animal (eg. sonar).



Figure 6. An autoradiograph of the superior colliculi of a monkey in which a radioactive marker had been injected in the retina. The marker (glowing brightly in this "dark field" micrograph) has been transported along the axons from the retina to the superficial laminae of the colliculus.



Figure 7. Low power micrograph of the intermediate grey (IG) and white (IW), and deep grey (DG) and white (DW) laminae of the superior colliculus, plus the periaqueductal grey (PAG).



Figure 8. Specific neuropeptides are found mainly in restricted layers, in this case substance P neurons in the superficial grey.





Figures 9,10. Large met-enkephalin neurons in the intermediate grey.



Figure 11. Bridging met-enkephalin axons between the intermediate grey and PAG.



Figure 12. Schema of the pain inhibitory pathway (from Bear MF, Connors BW, Paradiso MA, 2001. Neuroscience. Exploring the Brain. Second edition. Baltimore: Lippincott, Williams and Wilkins)

 


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