Telencephalic Connections in the Pacific Hagfish (Eptatretus Stouti)
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THE JOURNAL OF COMPARATIVE NEUROLOGY 395:245–260 (1998) Telencephalic Connections in the Pacific Hagfish (Eptatretus stouti), With Special Reference to the Thalamopallial System HELMUT WICHT1* AND R. GLENN NORTHCUTT2 1Klinikum der Johann Wolfgang Goethe-Universita¨t, Dr. Senckenbergische Anatomie, Institut fu¨ r Anatomie II (Experimentelle Neurobiologie), Theodor-Stern-Kai 7, 60590 Frankfurt, Federal Republic of Germany 2Neurobiology Unit, Scripps Institution of Oceanography and Department of Neurosciences, School of Medicine, University of California San Diego, La Jolla, California 9203-0201 ABSTRACT The pallium of hagfishes (myxinoids) is unique: It consists of a superficial ‘‘cortical’’ mantle of gray matter which is subdivided into several layers and fields, but it is not clear whether or how these subdivisions can be compared to those of other craniates, i.e., lampreys and gnathostomes. The pallium of hagfishes receives extensive secondary olfactory projec- tions (Wicht and Northcutt [1993] J. Comp. Neurol. 337:529–542), but there are no experimental data on its nonolfactory connections. We therefore investigated the pallial and dorsal thalamic connections of the Pacific hagfish. Injections of tracers into the pallium labeled many cells bilaterally in the olfactory bulbs. Other pallial afferents arise from the contralateral pallium, the dorsal thalamic nuclei, the preoptic region, and the posterior tubercular nuclei. Descending pallial efferents reach the preoptic region, the dorsal thalamus, and the mesencephalic tectum but not the motor or premotor centers of the brainstem. Injections of tracers into the dorsal thalamus confirmed the presence of reciprocal thalamopal- lial connections. In addition, these injections revealed that there is no ‘‘preferred’’ pallial target for the ascending thalamic fibers; instead, ascending thalamic and secondary olfactory projections overlap throughout the pallium. The mesencephalic tectum and tegmentum, which receive afferents from a variety of sensory sources, are interconnected with the dorsal thalamus; thus, ascending nonolfactory sensory information may reach myxinoid pallia via a tectal-thalamic-telencephalic route. A comparative analysis of pallial organization reveals that the subdivisions of the pallium in gnathostomes (i.e., medial, dorsal, and lateral pallia) cannot be recognized with certainty in hagfishes. J. Comp. Neurol. 395:245–260, 1998. 1998 Wiley-Liss, Inc. Indexing terms: myxinoidea; phylogeny; forebrain; pallium; diencephalon In amniotes, derivatives of the telencephalic pallium be rejected based on comparative data gathered in the last (i.e., the dorsal ventricular ridge in sauropsids and the two decades (reviewed in Northcutt, 1995). Ascending various cortical fields in mammals) are generally regarded sensory pathways reach the pallia of all gnathostomes as the ‘‘highest’’ integrative centers of the entire neuraxis. ( jawed craniates) investigated to date, and all gnathos- This is probably due to the fact that they are, at least in tomes display one or many pallial fields that receive no or humans, responsible for the transformation of reflectory only sparse secondary olfactory afferents from the olfac- sensorimotor activities into the conscious events of percep- tion, recognition, decision, and action. There is no direct line of pallial evolution ‘‘from fish to Grant sponsor: NIH; Grant numbers: NS24699/DC01081; Grant sponsor: man.’’ The earlier scenario of pallial evolution held that Dr. Senckenbergische Stiftung (Frankfurt/Main). primitive piscine pallia were entirely dominated by second- *Correspondence to: Helmut Wicht, Klinikum der Johann Wolfgang ary olfactory projections. An invasion of dorsal thalamic Goethe-Universita¨t, Dr. Senckenbergische Anatomie, Institut fu¨ r Anatomie II (Experimentelle Neurobiologie), Theodor-Stern-Kai 7, 60590 Frankfurt, fibers into the pallium was thought to have occurred in Federal Republic of Germany. E-mail: wicht@em.uni-frankfurt.de tetrapods, thus giving rise to the sensory pallial areas Received 23 September 1997; Revised 20 January 1998; Accepted 27 characteristic of mammals. This scenario, however, had to January 1998 1998 WILEY-LISS, INC. 246 H. WICHT AND R.G. NORTHCUTT tory bulb. Thus, it is highly likely that the pallium of the myxinoids is dominated by secondary olfactory projections common ancestor of all gnathostomes was not purely (Wicht and Northcutt, 1993). However, there are no data olfactory but contained separate pallial fields that were on its nonolfactory connections. It is therefore not clear dedicated to the processing of olfactory and ascending whether nonolfactory and, in particular, ascending tha- nonolfactory sensory information (Northcutt, 1995). lamic projections occur in myxinoids; nor is it clear whether However, the history of pallial evolution before the these projections, if they exist, have a particular pallial occurrence of gnathostomes is less clear. Recent studies in field as their target. In order to answer these questions, we jawless craniates (i.e., lampreys and hagfishes) have shed analyzed the connections of the pallium and the thalamus some light on the very early evolution of the pallium of the Pacific hagfish, Eptatretus stouti, by means of among craniates and have revealed substantial differences tract-tracing techniques. between jawless craniates and gnathostomes. Experimen- tal studies of the secondary olfactory projections in lam- preys (petromyzontids; Northcutt and Puzdrowski, 1988) MATERIALS AND METHODS have shown that these projections are indeed very exten- sive and reach all pallial fields, as predicted by the earlier Twenty-six adult and subadult Pacific hagfishes (Eptatre- scenario of pallial evolution. However, it has also been tus stouti, body length between 250 and 450 mm) were shown that the pallium of lampreys is not entirely olfac- used for this study. All animals were treated according to tory, because there is a substantial, presumably sensory, the guidelines outlined in the National Institutes of Health input from diencephalic and mesencephalic cell groups to Guide for the Care and Use of Laboratory Animals. The its medial subdivision (Polenova and Vesselkin, 1993; animals were caught in baited offshore traps near the Northcutt and Wicht, 1997). Scripps Institution of Oceanography (La Jolla, CA) and The pallium of the only other recent clade of jawless transferred into aquaria with running sea water at 10oC. craniates, the hagfishes (myxinoids), is highly differenti- Prior to any surgical manipulation the animals were ated from a cytoarchitectural point of view (Jansen, 1930; anesthetized with MS 222 (tricaine-methanesulfonate, Wicht and Northcutt, 1992). It consists of a superficial diluted 1:10,000 in sea water). ‘‘cortical’’ mantle of gray matter that is subdivided into The in vitro modification of the DiI technique (Godement various strata and fields, but it is not clear whether and et al., 1987) was used in three cases. In short, the how these subdivisions correspond to the medial, lateral, anesthetized animals were transcardially perfused with and dorsal subdivisions of the pallium of other craniates. 0.1 M phosphate-buffer (PB) at pH 7.4, followed by a Similar to the situation in lampreys, the pallium in freshly prepared solution of 4% paraformaldehyde (PFA) Abbreviations ’a’ nucleus ‘‘a’’ of Kusunoki P2 pallial layer 2 aol octavolateral area P2co compact part of pallial layer 2 ap area praetectalis P2l lateral part of pallial layer 2 BO olfactory bulb P2mc magnocellular part of pallial layer 2 BOg glomerular layer of BO P2pc parvocellular part of pallial layer 2 BOm mitral layer of BO P3 pallial layer 3 BOp periglomerular layer of BO P4l lateral part of pallial layer 4 cg central mesencephalic gray P4m medial part of pallial layer 4 coh habenular commissure P5 pallial layer 5 coib interbulbar commissure POe external preoptic nucleus copo postoptic commissure POim intermediate preoptic nucleus ctp commissure of the posterior tubercular area POp periventricular preoptic nucleus dcn dorsal column nuclei ra nuclei of the raphe Di diencephalon sIX,X sensory nucleus (lobe) of the glossopharyngeal and vagal fai internal arcuate fibers nerves fr fasciculus retroflexus sc spinal cord frs superior reticular formation sco subcommissural organ fri inferior reticular formation sp1 first spinal nerve gs posterior (‘‘saccular’’) octaval ganglion spocc spinooccipital nerve gu anterior (‘‘utricular’’) octaval ganglion st striatum gV trigeminal ganglion Ha habenula sV sensory nucleus of the trigeminus HYinf infundibular hypothalamic nucleus Tel telencephalon inp interpeduncular nucleus THa anterior nucleus of the thalamus lb bulbar lemniscus THdi diffuse nucleus of the thalamus mIX,X glossopharyngeal and vagal motor nucleus THe external nucleus of the thalamus Mes mesencephalon THi internal nucleus of the thalamus mV trigeminal motor nucleus THpco paracommissural nucleus of the thalamus nIX,X glossopharyngeal and vagal nerve THsh subhabenular nucleus of the thalamus nVII facial nerve THt triangular nucleus of the thalamus NCd dorsal nucleus of central prosencephalic complex tm mesencephalic tectum NCm medial nucleus of central prosencephalic complex TPl lateral nucleus of the posterior tubercular area NCvl ventrolateral nucleus of central prosencephalic complex TPm medial nucleus of the posterior tubercular area nflm nucleus of the medial longitudinal fascicle trolp deep part of the lateral olfactory tract nII optic nerve trols superficial part of the lateral olfactory tract nl olfactory nerve(s)