457
pattern of OE somata and dendrites seen in midshipman has not been reported in
other teleosts. Perhaps this brain area has not been examined closely in most other
species describing general CA fi ber distribution, or our fi ndings may refl ect a character specialization of sonic teleosts. Interestingly, in the European eel, which is
reported to produce sounds (Lagardere and Ernande 2004 ; Rountree et al. 2002 ),
varicose DA-ir fi bers as well as DA 1A/B and 2A/B receptors have been localized
to OE (Kapsimali et al. 2000 ; Pasqualini et al. 2009 ; Roberts et al. 1989 ). There are,
however, consistent reports of CA fi ber projections throughout the central auditory
system in fi shes. Studies in a diverse array of species such as sturgeon ( Acipenser ),
sea bass ( Dicentrarchus ), catfi sh ( Clarias ), stickleback ( Gasterosteus ), goldfi sh
( Carrassius ), zebrafi sh ( Danio ), African cichlid ( Astatotilapia ), European eel
( Anguilla ) electric fi sh ( Apteronotus and Gnathonemus ), and trout ( Oncorhynchus )
have reported TH-ir, DBH-ir and/or DA-ir fi bers and terminals in hindbrain octaval
nuclei, TS, CP, AT, and PGl (e.g., Adrio et al. 2002 ; Batten et al. 1993 ; Corio et al.
1991 ; Ekstrom et al. 1990 ; Ekstrom et al. 1986 ; Hornby and Piekut 1990 ; Kaslin
Fig. 6 (continued) auditory midbrain torus semicircularis (TS). Shown are nuclei interconnected
with TS. The dorsal thalamic central posterior nucleus (CP) contains reciprocal connections with
the ventral telencephalon (V; includes supracommissural division) and anterior hypothalamus (AT/
vT) (for nomenclature see Braford and Northcutt 1983 ). TS and CP also connect to vocal motor
nuclei in the forebrain (AT, vT, POA, not shown) and midbrain (PAG and isthmal/tegmentum, not
shown), while auditory-recipient octaval nuclei in the hindbrain connect to the VPG via the VPP
(also see Bass et al. 1994 ; Goodson and Bass 2002 ). The octavolateralis efferent nucleus (OE)
projects to the inner ear which includes the saccule, the main end organ of hearing (Bass et al.
1994 , 2000 ; Weeg et al. 2005 ). OE contains reciprocal connections with the VPP (Chagnaud et al.
2011 ) and receives projections from PAG (Kittelberger and Bass 2013 , not shown). Large, pearshaped TH-ir neurons from TPp send a massive dorsal turned descending tract into the hindbrain
which appears to innervate DO, SO, and OE and likely VMN. A branch of this tract exits the brain
via the efferent tract in the eighth nerve (VIII) to the inner ear. Other targets of TPp TH-ir neurons
include CP and PAG. The PAG and TPp are reciprocally connected (Kittelberger and Bass 2013 )
but whether PAG projects onto TH-ir cells in TPp is not confi rmed. TPp also has a robust ventral
ascending TH-ir projection although the exact innervation target in the ventral telencephalon (V)
is undetermined. See above references for additional known connectivity. ( b , c ) TH-ir innervation
of the saccule. ( b ) Section through the saccular epithelium (SE) including the attached branch of
VIII. The hair cell layer (HC) is delineated using the hair cell specifi c antibody (HCS-1, green )
which labels HC somata and can be distinguished from the basal support cells (SC) labeled by
DAPI ( blue ) alone. Thick and smooth TH-ir fi bers ( red ) course through VIII prior to terminating
largely at the base of the HC layer. Inset is lower magnifi cation of same section. ( c ) High magnifi -
cation image showing thick TH-ir varicose fi bers along the SC layer, fi ne-caliber terminals ( arrowheads ) at the base of the HC and less frequently terminals on the central portion of individual hair
cells proximal to the nucleus ( arrows ). ( d – f ) Neurobiotin backfi lls of the saccule combined with
TH immunofl uorescence identify source of TH-ir efferents to the saccular epithelium as a small
population of large, pear-shaped cells in the periventricular posterior tuberculum (TPp). ( d ) TH-ir
cells in the TPp just medial to the medial forebrain bundle and lateral and dorsal to the paraventricular organ. ( e ) Three neurobiotin-labeled neurons (two adjacent cells on top) after a saccular
backfi ll. ( f ) Overlay of images in a and b . Arrowheads indicate same cells and fi lled axons. All
neurobiotin-backfi lled cells in this region were also TH-ir. Adapted from Forlano et al. ( 2014 )
Neuroanatomical Evidence for Catecholamines as Modulators of Audition…
pattern of OE somata and dendrites seen in midshipman has not been reported in
other teleosts. Perhaps this brain area has not been examined closely in most other
species describing general CA fi ber distribution, or our fi ndings may refl ect a character specialization of sonic teleosts. Interestingly, in the European eel, which is
reported to produce sounds (Lagardere and Ernande 2004 ; Rountree et al. 2002 ),
varicose DA-ir fi bers as well as DA 1A/B and 2A/B receptors have been localized
to OE (Kapsimali et al. 2000 ; Pasqualini et al. 2009 ; Roberts et al. 1989 ). There are,
however, consistent reports of CA fi ber projections throughout the central auditory
system in fi shes. Studies in a diverse array of species such as sturgeon ( Acipenser ),
sea bass ( Dicentrarchus ), catfi sh ( Clarias ), stickleback ( Gasterosteus ), goldfi sh
( Carrassius ), zebrafi sh ( Danio ), African cichlid ( Astatotilapia ), European eel
( Anguilla ) electric fi sh ( Apteronotus and Gnathonemus ), and trout ( Oncorhynchus )
have reported TH-ir, DBH-ir and/or DA-ir fi bers and terminals in hindbrain octaval
nuclei, TS, CP, AT, and PGl (e.g., Adrio et al. 2002 ; Batten et al. 1993 ; Corio et al.
1991 ; Ekstrom et al. 1990 ; Ekstrom et al. 1986 ; Hornby and Piekut 1990 ; Kaslin
Fig. 6 (continued) auditory midbrain torus semicircularis (TS). Shown are nuclei interconnected
with TS. The dorsal thalamic central posterior nucleus (CP) contains reciprocal connections with
the ventral telencephalon (V; includes supracommissural division) and anterior hypothalamus (AT/
vT) (for nomenclature see Braford and Northcutt 1983 ). TS and CP also connect to vocal motor
nuclei in the forebrain (AT, vT, POA, not shown) and midbrain (PAG and isthmal/tegmentum, not
shown), while auditory-recipient octaval nuclei in the hindbrain connect to the VPG via the VPP
(also see Bass et al. 1994 ; Goodson and Bass 2002 ). The octavolateralis efferent nucleus (OE)
projects to the inner ear which includes the saccule, the main end organ of hearing (Bass et al.
1994 , 2000 ; Weeg et al. 2005 ). OE contains reciprocal connections with the VPP (Chagnaud et al.
2011 ) and receives projections from PAG (Kittelberger and Bass 2013 , not shown). Large, pearshaped TH-ir neurons from TPp send a massive dorsal turned descending tract into the hindbrain
which appears to innervate DO, SO, and OE and likely VMN. A branch of this tract exits the brain
via the efferent tract in the eighth nerve (VIII) to the inner ear. Other targets of TPp TH-ir neurons
include CP and PAG. The PAG and TPp are reciprocally connected (Kittelberger and Bass 2013 )
but whether PAG projects onto TH-ir cells in TPp is not confi rmed. TPp also has a robust ventral
ascending TH-ir projection although the exact innervation target in the ventral telencephalon (V)
is undetermined. See above references for additional known connectivity. ( b , c ) TH-ir innervation
of the saccule. ( b ) Section through the saccular epithelium (SE) including the attached branch of
VIII. The hair cell layer (HC) is delineated using the hair cell specifi c antibody (HCS-1, green )
which labels HC somata and can be distinguished from the basal support cells (SC) labeled by
DAPI ( blue ) alone. Thick and smooth TH-ir fi bers ( red ) course through VIII prior to terminating
largely at the base of the HC layer. Inset is lower magnifi cation of same section. ( c ) High magnifi -
cation image showing thick TH-ir varicose fi bers along the SC layer, fi ne-caliber terminals ( arrowheads ) at the base of the HC and less frequently terminals on the central portion of individual hair
cells proximal to the nucleus ( arrows ). ( d – f ) Neurobiotin backfi lls of the saccule combined with
TH immunofl uorescence identify source of TH-ir efferents to the saccular epithelium as a small
population of large, pear-shaped cells in the periventricular posterior tuberculum (TPp). ( d ) TH-ir
cells in the TPp just medial to the medial forebrain bundle and lateral and dorsal to the paraventricular organ. ( e ) Three neurobiotin-labeled neurons (two adjacent cells on top) after a saccular
backfi ll. ( f ) Overlay of images in a and b . Arrowheads indicate same cells and fi lled axons. All
neurobiotin-backfi lled cells in this region were also TH-ir. Adapted from Forlano et al. ( 2014 )
Neuroanatomical Evidence for Catecholamines as Modulators of Audition…