Organization of the ectostriatum based on afferent connections in the zebra finch (Taeniopygia guttata)

Brain Research 963 (2003) 101–112 www.elsevier.com / locate / brainres

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Organization of the ectostriatum based on afferent connections in the zebra finch (Taeniopygia guttata) Antonio V. Laverghetta 1 , Toru Shimizu* Department of Psychology, University of South Florida, PCD 4118 G, 4202 East Fowler Avenue, Tampa, FL 33620 -7200, USA Accepted 8 November 2002

Abstract In birds with laterally-located eyes, such as zebra finches and pigeons, the tectofugal visual pathway is the most prominent route from the retina to the telencephalon. However, little is known about exactly how the visual information is processed in this pathway, especially at the core region of the ectostriatum (Ec) in the telencephalon. In order to reveal a detailed organization of Ec, we decided to systematically analyze the afferent connections of Ec by injecting small amounts of sensitive tracers (biotinylated dextran amine and cholera toxin subunit B) selectively into different regions of Ec and the thalamic center of the tectofugal pathway (the nucleus rotundus, Rt). The present study revealed a clearer picture of the organization of Ec subdivisions than previously known. The present results showed that the anterior portion of Rt sent a heavy projection to the ventral region of the anterior Ec, whereas the more caudal subdivisions of Rt sent projections to more caudal and dorsal portions in Ec. The results suggest that Ec subdivisions appear to be arranged along an axis ‘rotated’ in the anterior direction, almost parallel to other major telencephalic laminae. These results may clarify the physiological and chemical heterogeneity of Ec found in the previous studies. The present findings also provide an insight into the possible organization of a visual processing center in a non-mammal.  2002 Elsevier Science B.V. All rights reserved. Theme: Other systems of the CNS Topic: Comparative neuroanatomy Keywords: Bird; Tract tracing; Visual pathway

1. Introduction In birds with laterally-located eyes, such as zebra finches and pigeons, the tectofugal visual pathway is the most prominent route from the retina to the telencephalon

[4,25]. This pathway travels from the retina to the optic tectum, then to the nucleus rotundus (Rt) of the dorsal thalamus, and finally to the ectostriatum of the telencephalon [1,18,23]. The ectostriatum is divided into a core region and a surrounding belt region. Only the core region (Ec) receives projections from Rt [18]. Previous studies

Abbreviations: 13, layer 13 of the tectum opticum; AL, ansa lenticularis; BDA, biotinylated dextran amine; Ce, central subdivision of the nucleus rotundus [18]; CO, cytochrome oxidase; CoA, anterior commissure; CTb, cholera toxin subunit B; Da, dorsoanterior subdivision of the nucleus rotundus [18]; DAB, 393-diaminobenzidine; DSV, decussatio supraoptica ventralis; Ec, ectostriatum core; FA, tracto fronto-archistriatalis; FPL, fasciculus prosencephali lateralis (lateral forebrain bundle); GLv, nucleus geniculatus lateralis, pars ventralis; HA, hyperstriatum accessorium; Hp, hippocampus; HV, hyperstriatum ventrale; LM, nucleus lentiformis mesencephali; LMD, lamina medullaris dorsalis; N, neostriatum; nBOR, nucleus of the basal optic root; NFL, lateral portion of the neostriatum frontale; NIL, lateral portion of the neostriatum caudale; OM, tractus occipitomesencephalicus; OV, nucleus ovoidalis; PA, paleostriatum augmentatum; PB, phosphate buffer; Post, posterior subdivision of the nucleus rotundus [18]; PP, paleostriatum primativum; PV, nucleus posteroventralis thalami; QF, tractus quintofrontalis; Rt, nucleus rotundus; SP, nucleus subpretectalis; T, nucleus triangularis; TeO, tectum opticum; TFM, tractus thalamo-frontalis et frontalis-thalamicus medialis; TPO, area temporo-parieto-occipitalis; TSM, tractus septomesencephalicus; TT, tractus tectothalamicus; VEP, visually evoked potential *Corresponding author. Tel.: 11-813-974-0352; fax: 11-813-974-4617. E-mail address: [email protected] (T. Shimizu). 1 Present address: Department of Anatomy and Neurobiology, University of Tennessee, Memphis, TN, USA. 0006-8993 / 02 / $ – see front matter  2002 Elsevier Science B.V. All rights reserved. PII: S0006-8993( 02 )03949-5

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showed that lesions in the tectofugal visual pathway cause severe deficits in various visual tasks, suggesting that this pathway plays a major role in color, brightness, and pattern discriminations [2,13–15]. However, little is known about exactly how the visual information is processed in the avian tectofugal pathway, especially at the forebrain level of Rt and Ec. Several lines of evidence have shown that the tectofugal pathway may be comprised of multiple subsystems. This suggests that processing visual information occurs in a parallel fashion, as it does in the visual system of primates. In particular, Rt appears to consist of multiple subdivisions based on anatomical and physiological studies. The Rt contains several cytoarchitectonically distinct subdivisions, although the exact number of the subdivisions is still uncertain [1]. Each of these Rt subdivisions appears to have distinct afferent connections with the optic tectum and efferent connections with Ec [1,10,11,19,23]. Histochemical studies showed that Rt can also be divided into subdivisions based on the staining intensity of different neurochemical contents, such as acetylcholinesterase [21] and a calcium-binding protein, calbindin [16]. Using electrophysiological methods, Wang and coworkers [29] showed that different regions of Rt have specific response characteristics. Thus, neurons in the anterior portion of Rt showed increased responses to changes in color and luminance, while those in the central and posterior portions showed increased responses to moving stimuli. Finally, lesion effects differ depending on the location of lesions within Rt. Lesions of the dorsoanterior portion caused significant deficits in a color discrimination task, whereas lesions of the central and posterior portions produce either minor or no deficits in the same task [20]. In contrast to Rt, the anatomical and functional organization of Ec has not been well understood. There are no obvious subdivisions and laminations on the basis of cytoarchitecture [24], morphology [26], or the distribution of several neurochemicals [5–8,27,28]. Nevertheless, there are at least two reasons to believe that discrete subdivisions exist in Ec, as in Rt. First, using retrograde tracers, tract-tracing experiments showed that separate portions of Ec receive efferent projections from different subdivisions of Rt [1,16,23]. The results of these connection studies suggest that the Rt–Ec connection is topographically organized, and that the functional segregation in Rt is maintained up to the level of Ec. Second, at least two previous studies have indicated heterogeneity within Ec. Hellman and coworkers [12] showed that the activity level of cytochrome oxidase (CO), an enzyme known to be indicative of metabolic activity, was not homogeneously distributed throughout Ec. The medial, dorsomedial, central, and ventrolateral regions in Ec showed high amounts of CO activity, whereas the centroventral and dorsolateral regions showed little CO activity. In addition, a density profile analysis of visually evoked potentials (VEPs) has indicated regional differences within Ec [9]. In particular,

the medioventral and rostrolateral portions of Ec showed marked VEP peaks in terms of latencies, suggesting that they may represent different stages of processing in Ec. These studies suggest that the potential parallel processing system in Rt may extend to Ec at the telencephalic level. In order to reveal a more detailed organization of Ec, we decided to systematically analyze the afferent connections of Ec by injecting small amounts of sensitive tracers selectively into different subdivisions of Rt and Ec. In particular, we thought that it was important to depict projection patterns from Rt subdivisions to Ec by conducting anterograde tract-tracing experiments. In regard to the subdivisions of Rt, we adopted the boundaries in the pigeon brain proposed by Mpodozis and his colleagues in the pigeon [22], who divided Rt into three regions: (1) the dorsoanterior (Da), (2) the central (Ce), and (3) the posterior (Post) divisions.

2. Materials and methods A total of 23 adult zebra finches of both sexes were used for this study. Among them, 11 subjects were used for the anterograde-tracing experiments, whereas 12 birds were used for retrograde-tracing experiments. The subjects in the anterograde-tracing experiment were subdivided into three groups according to the target of the tracer injection in the anterior, central, or posterior Rt. The subjects for the retrograde-tracing experiments received injections in different regions of Ec based on the results of the anterograde-tracing experiment. All methods used in the present study were carried out in accordance with the National Institute of Health Guide for the Care and Use of Laboratory Animals. Prior to surgery, the subjects were deprived of food for 30 min, with free access to water. The birds were deeply anesthetized with an intramuscular injection (i.m.) of nembutal (0.4 ml / 100 g body weight) and then placed in a stereotaxic device [3]. Stereotaxic coordinates of the injection site were determined using an atlas of the zebra finch brain (Bischof and Nixdorf, unpublished). According to the coordinate system based on this atlas, the sinus confluens was used as the zero point of the anterior– posterior axis, and the beak was positioned at 458 below the horizontal plane. In the anterograde-tracing experiment, subjects were unilaterally injected with a 10% solution of 10 000 Mr biotinylated dextran amine (BDA; Molecular Probes) in 0.01 M phosphate buffer (PB). The BDA was deposited iontophoretically using glass micropipettes with a tip size of 10–20 mm in diameter. The parameters of the injections were an intermittent anodal current of 4.5 mA for a duration of 5–15 s. The subjects in the retrogradetracing experiment received injections of either BDA or Cholera toxin subunit B (CTb). The CTb was injected using an air pressure system, with a pulse of 1–10 ms at 20 psi for each injection. After the surgery was complete,

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subjects were returned to their home cages with free access to food and water. After a survival period of 24 h, the subjects were killed with an overdose of nembutal (i.m.). The finches were perfused transcardially with 0.9% saline followed by icecold 4% paraformaldehyde in 0.1 M PB. The brains were removed and placed in 4% paraformaldehyde in PB for 16 h at 4 8C, followed by 30% sucrose in PB for at least 12 h for cryoprotection. The brains were frozen and cut in transverse sections at 40 mm on a sliding microtome. For BDA processing, brain sections were washed three times at 10 min each in PB at room temperature. The tissue was placed in vials on a rotator incubated in avidin–biotin reagent in 0.3% Triton X-100 in PB for 1 h at room temperature. The tissues were washed again in PB three times for 10 min each. To visualize the BDA, the tissues were incubated in 0.025% solutions of 39,3-diaminobenzidine (DAB). A solution of 0.3% hydrogen peroxide was then slowly added to obtain the brown reaction product. The tissues were then mounted on gelatin-coated slides and placed in a dust-free area to dry. The sections were dehydrated in an ethanol / xylazine series and coverslipped on glass slides with Permount. For CTb processing, the tissues were first incubated overnight at 4 8C in a solution of goat anti-CTb (1:10 000 dilution, LIST Laboratories). Tissues were then incubated in a solution of biotin conjugated anti-goat antiserum (1:200; Vector Laboratories), then in the avidin–biotin reagent, and reacted with DAB and hydrogen peroxide. Alternate sections from each experiment were stained with cresyl violet (Sigma) to visualize cell groups and neuronal structures. Tissues were microscopically examined using a macroscope and a microscope. The resulting images were drawn using a camera lucida or photographed using a scanning CCD camera. The drawn images were then scanned and saved using a graphic design program (Canvas 7). The photographed images were loaded in Adobe Photoshop software; only brightness and contrast were adjusted for the final images. In order to estimate the sizes of neurons in different Rt subdivisions, the perimeters of retrogradely labeled cells with CTb were drawn with a camera lucida. Only neurons with visible nuclei were selected. The drawings were then scanned and transferred to an NIH image analysis program to determine the areas for all neurons traced.

3. Results In Nissl-stained tissues, Rt of zebra finch is a round nucleus located in the dorsolateral region of the thalamus, containing larger cells than those in surrounding structures. The most rostral portion of Rt is designated as Da and appears just caudal to the nucleus lateralis anterior (Fig. 1A). Moving caudally, Rt as a whole becomes larger although Da occupies only the dorsal portion of the

Fig. 1. The three major subdivisions of Rt (Da, Ce, and Post) shown in selected transverse sections of the thalamus of the zebra finch from the rostral to caudal (A–D) levels. See list of abbreviations.

structure (Fig. 1B). Situated ventral to Da, Ce clearly consists of multiple subdivisions that differ cytoarchitectonically. The nucleus triangularis (T) appears dorsomedial to the caudal portion of Ce (Fig. 1C). The Post is the most

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caudal portion of Rt (Fig. 1D), which contains much smaller cells than Ce. However, the boundary between Ce and Post is not clear. The length of Rt along the anteroposterior axis is about 1.2 mm. In Nissl-stained tissues, Ec of the zebra finch is a large longitudinal structure, situated above the lamina medullaris

dorsalis (LMD). Containing densely packed cells, it appears just caudal to the nucleus basalis (see Figs. 2–4). Although there are no clear cytoarchitectonic subdivisions within Ec, the shape and location of Ec changes along the anteroposterior axis. The rostral and intermediate portion of Ec is a rectangular-shaped nucleus situated in the lateral

Fig. 2. (a) Brightfield photomicrograph showing the injection of BDA centered in Da at the location shown in A. Note that BDA is confined in Da, without spreading into Ce. (B–E) Anterograde labeling (fine dots) in Ec from the rostral to caudal levels following the injection depicted in A. See list of abbreviations.

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Fig. 3. (A) Depiction of the injection of BDA centered in Ce. (B–E) Anterograde labeling (fine dots) in Ec from the rostral to caudal levels following the injection depicted in A. See list of abbreviations.

portion of the telencephalon. At more caudal levels, Ec becomes narrower than the rostral Ec, extending medially and dorsally. The length of Ec along the anteroposterior axis is about 1.5 mm. Injections of BDA into Rt resulted in anterograde labeling limited to the ipsilateral Ec in the telencephalon, as well as in the contralateral Rt of the thalamus (not

shown here). In the telencephalon, the specific locations of terminal fields in Ec varied depending on injection sites within Rt along the rostrocaudal axis. When injections were largely confined to Da (Fig. 2A and a), a terminal field was found predominantly in the anterior Ec (Fig. 2B–E). Specifically, the heaviest labeling was seen in the most ventral portion of the anterior Ec, whereas only faint

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Fig. 4. (A) Depiction of the injection of BDA centered in Post. (B–E) Anterograde labeling (fine dots) in Ec from the rostral to caudal levels following the injection depicted in A. See list of abbreviations.

labeling was seen in the dorsal portion (Fig. 5A). As the sites of injections moved more caudally to Ce (Fig. 3A), terminal fields shifted caudally and dorsally to a central portion of the intermediate Ec (Figs. 3B–E). Such injections in Ce produced no labeled terminals in the most dorsal or the most ventral portions of Ec (Fig. 5B). Finally, injections centered in the most caudal division of Rt, Post

(Fig. 4A), produced terminal fields located further caudally and dorsomedially (Figs. 4B–E). The terminal fields following such injections in Post were predominantly in the most dorsal and medial portion of Ec whereas almost no labeling was seen in the ventral portion (Fig. 5C). Retrograde confirmation of Rt projections was made by injecting BDA or CTb into different portions of Ec. The

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results of the retrograde-tracing experiments were consistent with, and thus confirmed, the results of the anterograde-tracing experiments. In general, injections centered in each of the three Ec regions along the rostrocaudal axis (i.e. anterior, intermediate, and posterior parts of Ec) produced retrograde labeling in corresponding subdivisions of Rt (i.e. Da, Ce, and Post). At the same time, injections in different parts along the dorsoventral axis also influenced the labeling pattern in Rt. Thus, an injection centered into the most ventral portion of the anterior Ec produced retrograde labeled cells predominantly in Da (Fig. 6A), whereas an injection that was centered in a more dorsocaudal region (i.e. a dorsal region in the intermediate Ec) resulted in more labeled cells in Ce than Da (Fig. 6B). However, even when the injection was largely confined to the anterior Ec, if the tracer spread more dorsally, retrograde labeling was seen in Ce and Post as well (Figs. 6A and 7A). Conversely, even injections limited to the posterior Ec could produce labeled cell bodies in Da, if the injections included the most ventral portion of Ec (Figs. 6B and 7B). Injections of retrograde tracers in Ec also produced labeled cells in a nucleus in the ipsilateral hyperstriatum ventrale (not shown). Neurons in the nucleus triangularis were retrogradely labeled regardless of the different injection sites in Ec. Following injections of CTb in Ec, the areas of all retrogradely labeled cells in Rt were measured and analyzed between subdivisions (n5424 for Da, 585 for Ce, and 312 for Post). As shown in Figs. 8 and 9, the means of Da and Ce cells were almost identical (69.06 mm 2 , S.E.M.51.16 and 69.34 mm 2 , S.E.M.50.94, respectively), whereas the mean for Post was smaller than those (57.21 mm 2 , S.E.M.51.23). According to the overall analysis of variance, a difference among the subdivisions was statistically significant (F533.08, df52, P,0.001).

4. Discussion

Fig. 5. Photomicrographs showing terminal labeling in Ec at the intermediate level following the injections of BDA in Da (A), Ce (B), and Post (C). These injection sites were similar to those depicted in Figs. 2–4. Note that terminal labeling shifts dorsally in Ec (from A to C) as the injection sites move caudally from Da to Ce to Post. Contrast inverted to produce darkfield appearance. Scale bar51 mm. See list of abbreviations.

Consistent with previous studies [1,16,23], the present results showed that different subdivisions of Rt send projections to distinct portions of Ec. The present study also confirmed the observation that adjacent subdivisions of Rt project to adjacent portions of Ec, suggesting that the basic topographical organization of these subdivisions is maintained from Rt to Ec. Thus, the present study supports the notion that the parallel processing in Rt extends to the telencephalic level. The results of the present study have revealed a clearer picture of the organization of Ec subdivisions than previously known. By systematically analyzing the results of the anterograde- and retrograde-tracing experiments, the present results showed that Da sends a heavy projection to the ventral region of the anterior Ec, whereas the more caudal subdivisions of Rt send projections to more caudal and dorsal portions in Ec. Thus, as the source of the

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Fig. 6. Photomicrographs showing retrograde labeling in Rt following injections of CTb into Ec at the rostral level (A) and the intermediate level (B). Note that there are much more labeled cells in Da than in Ce following the injection in the rostral Ec (A) whereas the opposite is the case following the injection in the more caudal injection (B). See list of abbreviations.

ascending projection moves caudally in Rt, the target of the projection in Ec shifts caudodorsally. These projection patterns from Rt suggest that the subdivisions of Ec are organized along the anterior–posterior axis. This axis is not exactly parallel to the horizontal plane used in the coordinate system of the present study. Rather, the Ec subdivisions appear to be arranged along an axis ‘rotated’ in the anterior direction, almost parallel to other major telencephalic laminae, such as the lamina hyperstriatica (LH) and LMD (Fig. 10). Because of this ‘rotation,’ different subdivisions of Ec can sometimes be seen in the same transverse section, as exemplified in photographs of Fig. 5. In Fig. 10, a section with an asterisk schematically represents such a section. Because of the lack of clear cytoarchitectonic borders, it is difficult to see heterogeneity in Ec. However, the concept of a ‘rotated’ organization of Ec subdivisions may clarify findings from previous studies about physiological and chemical heterogeneity in Ec [9,12]. These studies showed differences between regions in Ec along the dorsoventral axis, as well as the anteroposterior axis. These previous studies and the present study used similar coordinate systems (finches [3] and pigeons [17]), in which the beak (i.e. the anterior fixation point) is placed 458 below the horizontal plane defined by the ear bar of the stereotaxic instrument (i.e. the posterior fixation point). Therefore, in these studies, as in the present study, different subdivisions of Ec might have appeared along the dorsoventral axis in same sections. For instance, previous electrophysiological data [9] showed regional differences within Ec of zebra finches. In particular, the medioventral and rostrolateral portions of Ec have been suggested to be distinguished from the rest of Ec. These two areas may correspond to the central and ventroanterior portions of Ec in the present study, each of which receives a projection from Ce and Da subdivisions of Rt, respectively. Similarly, the centroventral and dor-

solateral regions of Ec show distinctively lower CO activity compared to the rest [12]. This may correspond to the central and ventroanterior portions of Ec in the present study. Although the subject species used in these studies are different (i.e. pigeons [12], finches [9], present study), it is likely that Ec of finches and pigeons are similarly organized since the same basic organization pattern has been reported in Rt of both species [1,23]. The present findings also provide insight about the possible organization of avian telencephalic structures in general. Due to the apparent lack of a cortex-like laminar structure, the avian telencephalon appears to consist of an aggregation of nuclear masses [25]. For instance, Ec first appears to be an odd-shaped nucleus incongruously embedded in the neostriatum. However, the present results suggest a possibility that the telencephalic nuclei, such as Ec, are arranged in a more ‘laminar’ fashion than previously considered. Thus, the results showed that the axis of Ec subdivisions is ‘rotated,’ just as other laminae in the telencephalon, and that individual Ec subdivisions are arranged almost perpendicular to this axis (Fig. 10). A previous study [16] has shown that different regions of Ec along the anteroposterior axis have topographically organized projections, which ultimately terminate in the outmost edge of the telencephalon (designated as the pallium externum by Veenman and coworkers [27,28]). The anterior portion of Ec first sends projections to the anterior portion of the surrounding belt region, which in turn projects primarily to the anterior portion of the pallium externum (the lateral portion of the neostriatum frontale, NFL). Similarly, the intermediate portion of Ec projects to the intermediate belt region, which then sends major projections to the intermediate portion of the pallium externum (the area temporo-parieto-occipitalis, TPO). Finally, the caudal Ec projects to the caudal belt region, which projects primarily to the caudal portion of the pallium externum (the lateral portion of the neostriatum

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Fig. 7. (A) Retrograde labeling (bold dots) in Rt following the injection of CTb in the anterior Ec depicted in the top figure. Note that there are labeled cells in Ce and Post, as well as Da, following the injection that included the dorsal portion of Ec. (B) Retrograde labeling in Rt following the injection of BDA in the caudal Ec depicted in top figure. Note that there are labeled cells in Da, as well as Ce and Post, following the injection that included the ventral portion of Ec. See list of abbreviations.

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Fig. 9. The graph represents the areas of retrogradely labeled cells in the three Rt subdivisions following CTb injections in Ec. Values are expressed as means6S.E.M.

Fig. 8. Photomicrographs showing retrogradely labeled cells in Da (A), Ce (B), and Post (C) following the injections of CTb in Ec. Note that labeled cells in Post (C) are smaller than those in the more anterior subdivisions (A and B). Scale bar5100 mm.

‘laminar’ view of Ec may be worth considering since visual information is processed in a columnar organization in the mammalian cortex. Finally, another new finding of this study is the size differences of neurons between subdivisions of Rt. Cells in Da and Ce are larger than those in Post. These results are intriguing when the functional segregation of Rt subdivisions is considered. Wang and colleagues [29] suggested that neurons of Da may be specialized for color processing, whereas those in Ce and Post may be specialized for motion perception. This is especially true for the most caudal portion of Rt, as it has been suggested to be involved in the perception of ‘looming’ stimuli, or movement in three dimensions. The present results are somewhat puzzling when compared with the mammalian data, if neuronal size is indeed related to the properties of circuits for processing different aspects of the visual world. In the lateral geniculate nucleus of mammals, neurons for motion perception are known to be larger than those for color and form perception. It is possible that the finch Rt may be differently organized, or that motion perception in Rt cannot be compared directly to that in the mammalian thalamus.

Acknowledgements intermediale, NIL). These observations suggest that Ec can be interpreted as a part of the neostriatal region located between telencephalic lamina (i.e. LH and LMD) and that different subdivisions of Ec may correspond to ‘columns’ that have distinct connections with other telencephalic areas, such as NFL, TPO, and NIL. Further studies of Ec organization and other telencephalic structures are essential to determine whether this view is valid. Nevertheless, this

The authors are grateful to Scott Husband and Anton Reiner for their comments on the manuscript. The stereotaxic apparatus and brain atlas were generously donated by Dr. Hans-Joachim Bischof. This study was supported by a Research and Creative Scholarship Grant from University of South Florida and a research grant from the National Science Foundation to T.S. (IBN-0091869).

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Fig. 10. Schematic diagram summarizing the connections delineated in the present study. See list of abbreviations.

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