Electroreceptive Mechanisms in the Platypus

this page contains information on the receptors, afferent pathways and central representation of electroreception in the platypus.

Electroreception would seem to be an extremely useful means to detect and hunt prey. Manger and Pettigrew (1995) studied the platypus electroreceptive system and its relation to hunting behavior in the platypus. It appears that platypus spent up to 40% of its time searching for food. The platypus search for food by swinging their heads back and forth, presumably attempting to detect electrical fields emitted by movement of their prey (see the behavior link for more details). They believe that a head movement saccade initiated by an electric stimuli demonstrates the importance of electroreception in platypus hunting. However, this may or may not be the case; Taylor, Manger, Pettigrew and Hall (1992) compared the electromyogenic potentials produced by platypus prey with platypus electroreceptive capabilities. They conclude that it seems "unlikely that electroreception could play a teloreceptive role in guiding the platypus towards... prey," and instead suggest "the electroreceptive system... could facilitate the mechanical stimulation resulting from direct contact with the prey" (p. 223). Thus, the exact use of the electroreceptive system in platypus hunting has not yet been agreed upon.

Peripheral Electroreceptors...

While all three fish electroreceptive systems found to date employ a sensory cell in the periphery to collect electrosensory stimuli (e.g. the Knollenorgan of mormyrid electric fishes), the platypus appears to exhibit no special sensory cells whatsoever (for more information on electroreception in fish, see Species Recognition in Electric Fish, Jamming Avoidance Response in Electric Fish, and Hormonal Control of Electric Organ Discharge). Instead, electrical signals are collected by bare nerve endings buried in modified mucous glands.

(all information in the next two paragraphs was derived from Manger, Pettigrew, Keast and Bauer 1995, and can be found as a figure). These glands have three layers of tissue surrounding the actual lumen of the gland. The layer most proximal to the lumen in known as the periluminal layer, and is composed of 2-3 layers of loosely packed keratinocyte cells. The second layer, more distal to the lumen than the periluminal layer, is called the dense zone; it is composed of 7-10 layers of tightly packed flatten keratinocytes. The dense zone has been found to exhibit many tight junctions between cells. Finally, the germanitive zone is most distal to the lumen, and has been found to be characterized by 2-3 layers of cells.

An average of 16 nerve terminals have been found in each modified mucous gland. A large terminal bulb for each of the 16 neurons is found in the germinative zone. This bulb represents a distal portion of the dendritic projection to the mucous gland. The projection continues further to a small bulb between the germinitive and dense zones; the small bulb projects the most distal dendritic fiber, the terminal filament, into the periluminal zone. This terminal fiber is the actual bare nerve terminal that appears to conduct electrosensory information in the monotremes. However, it is important to note that the filament does not actually reach the lumen: the most distal portion of any of the 16 terminal filaments are still about 20 um from the mucosal lumen. This finding begs the question, how is the electric signal coneyed through the perilumenal layer to the terminal filament?

Manger, Pettigrew, Keast and Bauer (1995) believe the dense layer, being densely packed with cells and tight junctions, represents a high-resistance insulator that forces any current passing through the perilumenal layer into the terminal fibers (which are low resistance). Correspondingly, Manger et al. believe the perilumenal layer is low resistence, as it is very loosely-packed. Thus current from the external enviornment is conducted through the mucosal lumen to the perilumenal zone, where it is picked up by the terminal fibers and passed downstream via the small, then large bulbs in the germinative zone.

I would like to emphasize that Manger, Pettigrew, Keast and Bauer's proposal is, at this time, still just a theory. There has been no recent work to substantiate this prediction. In addition, there is one additional problem that requires explanation (although Manger et al. do have a few possible explanations): what prevents the current from bypassing the periluminal zone, and instead simply continuing up the mucosal lumen?

Afferent Pathways...

Nerve terminals leaving the bill project entirely to the trigeminal nerve, through the ventral basal complex of the thalamus, and eventually arrive at the primary somatosensory cortex.  The trigeminal nerve has been found to contain axon proportion approximately equal to the proportion of different kinds of receptors on the surface of the bill (Manger and Pettigrew, 1996).

Central Projections...

Krubitzer et al. (1995) found that electroreceptive projections form a topographic map that is intermixed with the somatosensory cortical map of the bill. The bill representation is extremely large, monopolizing up to one half of the extent of the cortex (Manger, Calford and Pettigrew. 1996).  The bill is represented contralaterally, as are all cortical sensory representations. In addition, the actual topographic map is oriented such that distal portions of the bill are represented laterally, and lateral portions of the bill represented caudally (Proske, Iggo, McIntyre, Gregory. 1993).

Electrophysiological work has demonstrated separate, but interdigitating strips of cells, one only responsive to cutaneous stimulation, the other sensitive to both cutaneous and electrical stimuli. Furthermore, it was found that tactile-sensitive cells stained cytochrome oxidase upon reaction, while the elecro- and tactile -sensitive cells stained CO-light (Krubitzer, et al. 1995).  Cortical processing of electrosensory data therefore occurs in these CO-light multimodal strips of somatosensory cortex. Krubitzer, et al. (1995) also noted that electrosensory afferents from the bill projected to several different regions in the CO-light cortical strips, representing each electroreceptor several times in the cortex. These rerepresentations formed modules of cortical neurons responding, at various thresholds, to the same peripheral location--thus, collectively, the modules contain mutliple representations of the bill's electroreceptors, all of varying threshold values.  These different threshold levels ranging from 50 uV/cm to 200 uV/cm; however, each individual neuron had a very limited dynamic range, most saturating within 20 uV/cm of their threshold (Manger, Calford and Pettigrew 1996). This 20 uV/cm range is narrow enough relative to the system at hand that "they can be considered as having only two states: inactive and saturated (Manger, Calford and Pettigrew, p. 615)." Cortical positions representing different peripheral locations were always in different portions of the CO-light multimodal cortex, but usually adjacent to one another. Furthermore, these cortical neurons have very low levels of spontaneous activity.

Thus, platypus primary somatosensory cortex contains repeated rerepresenations of the elecro- and tactile-sensitive inputs of the bill, each rerepresentation demonstrating a unique threshold that is reached, and saturated, almost instantly.  It is the opinion of Manger, Calford and Pettigrew that the decay patterns of electrical fields across the bill would be encoded by processing two variables: which neurons respond in which representation modules. A given cortical cell will only respond to a stimuli if the stimulus is above its threshold within its receptive field.  A field falling across the bill induces  receptors closer to the source to respond with greater vigor than then repeptors farther from the source. Therefore, in the cortex, more neurons would fire in the modules representing the proximal side of the bill than the distal because more neurons of higher threshold values would be active. On the distal side, only those neurons whose threshold values were low enough to be stimulated by the distant elctrical source would fire. Thus, by noting the gradient in populations recruited to represent different stimuli, the platypus can determine the direction of the elecric field. Similarly, by noting the absolute number of cortical neurons firing to given stimulus, the animal can determine the intensity of the actual elecrical field.

Given an electrical stimulus, the absolute number and distribution of activated poputlations will indicate how intense the stimulus, giving some kind of relative indication of distance. As the field decays across the electrosensitive platypus bill, the electroreceptors most proximal to the stimulus will receive a more intense stimulus. More cortical neurons whose receptive fields are proximal to the stimulus will have reached saturation in more modules, all at different threshold values. However, cortical neurons whose receptive fields are distal to the stimulus will have only reached saturation in the few modules where their threshold is low enough. Therefore, direction of the stimulus will be encoded in the pattern of decreasing activity along one vector or another. To quote Manger, Calford and Pettigrew, "the pattern of activity produced by a given stimulus will topographical encode the direction of the origin of the stimulus in terms of the relative activation pattern of the modules" (p. 615).

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