This was the first detailed ultrastructural study of the neuromuscular junctions of larval Drosophila, now being used increasingly to study genetic effects on neurotransmission.
 

2. Wojtowicz, J.M., Atwood, H.L. and Marin, L. (1994) Activity-induced changes in synaptic release sites in the crayfish neuromuscular junction. Journal of Neuroscience 14:3688- 3703.

This paper introduces a new method for identifying synapses in the electron microscope after electrical recordings have been made from them to study their properties of transmitter release. We provide evidence that not all synapses on a nerve terminal are involved in release at low frequencies, and that the number participating in release increases with frequency of activity. A form of long-term potentiation is correlated with an increase in the number of structurally complex synapses (multiple active zones), indicating that structural modification of synapses contributes to prolonged enhancement of transmitter release.
 

3. Nguyen, P.V. and Atwood, H.L. (1994) Altered impulse activity modifies synaptic physiology and mitochondria in crayfish motor neurons. Journal of Neurophysiology 72:2944- 2955.

Long-term adaptation of neurotransmission and structure in identified phasic neurons to altered activity is accompanied by modifications in mitochondria which increase their potential to generate ATP. This change is correlated with, and probably responsible for, the elevated resistance to synaptic depression that occurs consequent to increased activity in the neuron.
 

4. Stewart, B.A., Atwood, H.L., Renger, J.J., Wang, J., and Wu, C.-F. (1994) Improved stability of Drosophila  larval neuromuscular preparations in haemolymph-like physiological solutions. Journal of Comparative Physiology 175,   179-191.

We developed a new physiological solution for physiological studies of Drosophila preparations. We found that the solution previously in use causes rapid damage to the preparations, resulting in unstable physiology.
 

5. Kurdyak, P., Atwood, H.L., Stewart, B.A., and Wu, C.-F. (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. Journal of Comparative Neurology 350, 463-472.

The physiological differences in synaptic transmission of two motor neurons to a Drosophila larval muscle were critically defined for the first time.
 

6. Cooper, R.L., Marin, L. and Atwood, H.L. (1995) Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure. Journal of Neuroscience 15:4209-4222.

Diffferent terminals of the same neuron release widely different amounts of neurotransmitter per impulse. This is linked to a larger calcium entry at high-output terminals. The number of synapses does not differ in the two terminal types, but there are more complex synapses in the high-output terminal. Quantal analysis indicates a higher probability of release for responding synapses in high-output terminals, and this is likely linked to the higher calcium entry.
 

7. Shupliakov, O., Atwood, H.L., Otterson, O.P., Storm- Mathisen, J. and Brodin, L. (1995) Presynaptic glutamate levels in tonic and phasic motor axons: correlation with properties of synaptic transmission. Journal of Neuroscience 15:7168-7180.

This collaborative study was a successful effort to characterize molecular differences in phasic and tonic nerve endings by means of immunocytochemical methods at the electon microscopic level. We demonstrated that the levels of free and mitochondrion-associated glutamate (the transmitter in these neurons) are twice as high in tonic as in phasic terminals. This leads to an hypothesis for regulation of glutamate levels as a factor in synaptic vesicle replenishment, which could play a role in the relative resistance of tonic neurons to synaptic depression.
 

8. Cooper, R.L., Hampson, D.R. and Atwood, H.L. (1995) Synaptotagmin-like expression in the motor nerve terminals of crayfish. Brain Research 703:214-216.

In this short preliminary report, we provide the first demonstration that an antibody to a Drosophila synaptic protein reacts strongly with its crustacean counterpart. The observation confirms that it is feasible to consider using discoveries at the molecular level in Drosophila for investigations of the physiologically more amenable crustacean synapses.

9. Cooper, R.L., Winslow, J., Govind, C.K. and Atwood, H.L. (1996) Synaptic structural complexity as a factor enhancing probability of calcium-mediated transmitter release. Journal of Neurophysiology 75: 2451-2466.

In this paper, we draw upon our observations of crustacean synapses (based upon serial reconstructions from electron micrographs, and freeze-fracture replicas of active zones) to develop a mathematical model of calcium entry and distribution following a nerve impulse. We test the hypothesis that synapses with two active zones are more likely to release transmitter due to interaction of their localized calcium domains. This provides a mechanism for synaptic recruitment within the nervous system.
 

10. Stewart, B.A., Schuster, C.M., Goodman, C.S. and Atwood, H.L. (1996) Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. Journal of Neuroscience 16: 3877-3886.

We show that synapses can adapt to compensate for genetic defects, maintaining normal synaptic transmission.
 

11. Karunanithi, S., Georgiou, J., Charlton, M.P. and Atwood, H.L. (1998) Imaging of calcium in Drosophila larval motor nerve terminals. Journal of Neurophysiology, 78: 3465-3467.

We show the feasibility of intracellular calcium measurements in Drosophila nerve terminals during synaptic transmission. This method can be used in genetic studies of neurotransmission.

12. Kennedy, K.M., Piper, S.T., and Atwood, H.L. (1999) Effectiveness of single-channel Ca2+ for synaptic vesicle recruitment examined by Monte Carlo simulation at the crayfish neuromuscular junction. Canadian Journal of Physiology and Pharmacology 77: 634-650.

Theoretical treatment of calcium entry and transmitter release.

13. Msghina, M., Millar, A.G., Charlton, M.P., Govind, C.K., and Atwood, H.L. (1999) Calcium entry related to active zones and differences in transmitter release at phasic and tonic synapses. Journal of Neuroscience 19: 8419-8434.

Differences in calcium sensitivity are considered to be responsible for large diffrences in synaptic transmission.

14. Dawson-Scully, K., Bronk, P., Atwood, H.L., and Zinsmaier,  K.E. (2000) Cysteine-string protein increases the calcium sensitivity of late steps in  fast neurotransmitter exocytosis. Journal of Neuroscience 20: 6039-6047.

Cysteine string protein mutants do not exhibit loss of Ca²⁺ entry at synapses, ut instead exhibit loss of Ca²⁺ sensitivity.

 

15. Millar, A.G., Bradacs,. H., Charlton, M.P., and ATwood, H.L. (2002) Inverse relationship between release probability and readily releasable vesicles in depressing and facilitating synapses. Journal of Neuroscience 22: 9661-9667.

Synaptic vesicles stores are larger in tonic than in phasic crayfish motor synapses, althought trnasmission is much stronger initally in phasic terminals.

16. Macleod, G.T., Hegström-Wojtowicz, M., Charlton, M.P., and Atwood, H.L. (2002) Fast calcium signals in Drosophila motorneuron terminals. Journal of Neurophysiol. 88: 2659-2663.

New procedures for analyzing synaptic transmission in Drosophila.

17. Song, W., Ranjan, R., Bronk, P., Dawson-Scully, K., Marin, L., Seroude, L.; Lin, Y.-J., Nie, Z., Atwood, H.L., Benzer, S., and Zinsmaier, K.E. (2002). Presynaptic regulation of neurotransmission in Drosophila by the G protein-coupled receptor Methuselah. Neuron 36: 105-119.

Describes physiological roles for a G protein-coupled receptor known to regulate life span in Drosophila.

18. Millar, A.G., Bradacs, H., Charlton, M.P., and Atwood, H.L. (2002) Inverse relationship between release probability and readily releasable vesicles in depressing and facilitating synapses. Journal of Neuroscience 22: 9661-9667.

This study shows that probability of synaptic vesicle release distinguishes two types of synapse.

19. Karunanithi, S., Marin, L., Wong, K., and Atwood, H.L. (2002) Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. Journal of Neuroscience 22, 10267-10276.

Size of the unitary (quantal) event in synaptic trnasmission is related to size of synaptic vesicles.

20. Macleod, G.T., Suster, M.L., Charlton, M.P., and Atwood, H.L. (2003) Single neuron activity in the Drosophila larval CNS detected with calcium indicators. Journal of Neuroscience Methods 127, 167-178.

Optical methods for investigating nerve cell activity in the ceantral nervous system.

21. Millar, A.G. and Atwood, H.L. (2004) Crustacean phasic and tonic motor neurons. Integrative and Comparative Biology 44, 4-13.

Review of the features of two types of synapse in crustaceans.

22. Macleod, G.T., Marin, L., Charlton, M.P., and Atwood, H.L. (2004) Synaptic vesicles: Test for a role in presynaptic calcium regulation. Journal of Neuroscience 24, 2496-2505.

A proof that synaptic vesicles do not regulate calcium channels or calcium extrusion dynamics in presynaptic nerve terminals.

23. Millar, A.G., Zucker, R.S., Ellis-Davies, G.C.R., Charlton, M.P. and Harold L. Atwood (2005) Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses. Journal of Neuroscience 25: 3113-3125.

Direct proof of a difference in calcium sensitivity in two types of synapse.

24. Bronk, P., Nie, Z., Klose, M.K., Dawson-Scully, K., Zhang, J., Robertson, R.M., Atwood, H.L., and Zinsmaier, K.E. (2005) Multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. Journal of Neuroscience 25:2204-2214.

Different domains of the cysteine-string protein have distinct functions.

25. Guo, X., Macleod, G.T., Wellington, A., Hu, F., Panchumarthi, S., Schoenfield, M., Marin, L., Charlton, M.P., Atwood, H.L., and Zinsmaier, K.E. (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47: 379-393.

A mutant lacking mitochondria in nerve terminals can maintain synaptic function.

26. Cheung, U., Atwood, H.L., and Zucker, R.S. (2005) Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. Journal of Neurobiology (accepted for publication).

27. Neal, S.J., Karunanithi, S., Best, A., So, A.K.-C., Tanguay, R.M., Atwood, H.L., and Westwood, J.T. (2005) Thermoprotection of synaptic transmission in a Drosophila heat shock factor mutant is accompanied by increased expression of Hsp83 and Hsp40. Physiological Genomics (submitted).

28. Romero-Pozuelo, J., Dason, J.S., Atwood,H.L. and Ferrús, A. (2005) Effects of altered levels of two frequenin genes on synaptic transmission at the Drosophila larval neuromuscular junction. (submitted).

1. Atwood, H.L. (1963) Differences in muscle fibre properties as a factor in "fast" and "slow" contraction in Carcinus. Comparative Biochemistry and Physiology, 10, pp. 17-32.

The first observations on physiological differentiation of muscle fiber properties in crustacean limb muscles, explaining features of the differences in contractions elicited by different motor axons.
 

2. Atwood, H.L., Hoyle, G. and Smyth, T. (1965) Mechanical and electrical responses of single innervated crab-muscle fibres. Journal of Physiology (London), 180, pp. 449-482.

The relationship between synaptic transmission and muscle contraction was defined for crustacean muscles through studies of single innervated muscle fibers.

3. Atwood, H.L. (1967) Variation in physiological properties of crustacean motor synapses. Nature, London, 215, pp. 57-58.

The first report on the presynaptic basis of 'strong' and 'weak' synapses of a single neuron.
 

4. Sherman, R.G. and Atwood, H.L. (1971) Synaptic facilitation: Long-term neuromuscular facilitation in crustacean muscles. Science, 171, pp. 1248-1250.

The first report on long-term facilitation (a form of long- term potentiation).
 

5. Jahromi, S.S. and Atwood, H.L. (1974) Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. Journal of Cell Biology, 63, pp. 599-613.

The first 3-dimensional characterization of crustacean neuromuscular junctions, 'active zones', and possible 'silent' synapses.
 

6. Atwood, H.L., Swenarchuk, L.E. and Gruenwald, C.R. (1975) Long-term synaptic facilitation during sodium accumulation in nerve terminals. Brain Research, 100, pp. 198-204.

Ionic events linked to long-term facilitation were analyzed.
 

7. Atwood, H.L., Govind, C.K. and Kwan, I. (1977) Non- homogeneous excitatory synapses of a crab stomach muscle. Journal of Neurobiology, 9, pp. 17-28.

Ultrastructural basis for 'strong' and 'weak' synapses examined; synaptic complexity varies among individual synapses of a single terminal.
 

8. Lnenicka, G.A. and Atwood, H.L. (1985) Age-dependent long-term adaptation of crayfish phasic motor axon synapses to altered activity. Journal of Neuroscience, 5, pp. 459-467.

First description of long-term adaptation of synaptic transmission due to altered neural activity.
 

9. Wojtowicz, J.M. and Atwood, H.L. (1986) Long-term facilitation alters transmitter releasing properties at the crayfish neuromuscular junction. Journal of Neurophysiology, 55, pp. 484-498.

First quantal analysis of long-term facilitation; evidence for new synapses being recruited to enhance synaptic transmission.
 

10. Lnenicka, G.A., Atwood, H.L. and Marin, L. (1986) Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation. Journal of Neuroscience, 6, pp. 2252-2258.

First description of morphological transformation of synaptic terminals by altered activity. Synapses adapt to meet the demands of activity.
 

11. Wojtowicz, J.M. and Atwood, H.L. (1988) Presynaptic long-term facilitation at the crayfish neuromuscular junction: voltage-dependent and ion-dependent phases. Journal of Neuroscience, 8, pp. 4667-4674.

Detailed analysis of ionic events necessary for long-term facilitation; calcium entry is not required for maintained enhancement of transmission.
 

12. Dixon, D. and Atwood, H.L. (1989) Adenylate cyclase system is essential for long-term facilitation at the crayfish  neuromuscular junction. Journal of Neuroscience, 9, pp. 4246-4252.

Requirement of cAMP for long-term facilitation in crayfish terminals.
 

13. Nguyen, P.V. and Atwood, H.L. (1990) Expression of long-term adaptation of synaptic transmission requires a critical period of protein synthesis. Journal of Neuroscience, 10, pp. 1099-1109.

Timed protein synthesis needed for neuronal adaptation to activity.
 
 
 

 1. Atwood, H.L. and MacKay, W.A. (1989) "Essentials of Neurophysiology" B.C. Decker Inc., Toronto and   Philadephia, pp. 1-405.

 2. Atwood, H.L. and Nguyen, P.V. (1990) Physiological properties of crustacean motor neurons and the alteration of these properties. In "Frontiers of Crustacean Neurobiology", ed. K. Wiese; Birkhauser-Verlag AG, Basel, pp. 345-350.

3. Atwood, H.L., Nguyen, P.V., and Mercier, A.J. (1991) Activity-dependent adaptation in neuromuscular systems. In "Plasticity of Motoneuronal Connections", Restorative Neurology, volume 5, ed. A. Wernig; Elsevier Science Publishers BV, Amsterdam, pp. 101-114

4. Atwood, H. L. (1992) Age-dependent alterations of synaptic performance and plasticity in crustacean motor systems. Experimental Gerontology, 27, 51-61

5. Atwood, H.L. and Tse, F.W.Y. (1993) Physiological aspects of presynaptic inhibition. Advances in Neural Science 1, 19-65.

6. Atwood, H.L., Cooper, R.L., and Wojtowicz, J.M. (1994) Non-uniformity and plasticity of quantal release at crustacean motor nerve terminals. Advances in Second Messenger and Phosphoprotein Research (ed. Stjärne, L. Greengard, R., Grillner, S., Hökfelt, T., and Ottoson, D.) 29, 363-382.

7. Atwood, H.L., and MacKay, W.A. (1994) Neurophysiologie: Text-Bild-Manual. (Deutsche Übersetzung und Bearbeitung, Jörg Walden and Otto V. Witte). Schattauer: Stuttgart-New York, 403 pp.

8. Atwood, H.L., and Nguyen, P.V. (1995) Neuronal adaptation in crayfish. American Zoologist, 35:28-36.

9. Atwood, H.L., and Cooper, R.L. (1995) Functional and structural parallels in crustacean and Drosophila neuromuscular systems. American Zoologist, 35: 556-565.

10. Atwood, H.L. and Cooper, R.L. (1996) Assessing ultrastructure of crustacean and insect neuromuscular junctions. Journal of Neuroscience Methods 69: 51-58.

11. Atwood, H.L. and Cooper, R.L. (1996) Synaptic diversity and differentiation: crustacean neuromuscular junctions. Invertebrate Neuroscience 1: 291-307.

12. Atwood, H.L., Karunanithi, S., Georgiou, J. and Charlton, M.P. (1997) Strength of synaptic transmission at neuromuscular junctions of crustaceans and insects in relation to calcium entry. Proceedings of the 5th International Conference on Invertebrate Neurochemistry and Neurophysiology. Invertebrate Neuroscience 3, 81-87.

13. Atwood, H.L., Kennedy, K., and Msghina, M. (1998) Regulation of transmitter release at synapses of single identified crustacean neurons. Human Frontiers Science Program, Workshop IV, "Central Synapses: Quantal Mechanisms and Plasticity". (eds. Faber, D., Korn, H., Redman, S., Thompson, S., and Altman, J.S.), pp. 73-82.

14. Atwood, H.L. and Wojtowicz, J.M. (1999) Silent synapses in neural plasticity: current evidence. Learning &     Memory, 6: 542-571.

15. Atwood, H.L. (2002) Deteminants of Synaptic Strength and Stability at Crustacean Neuromuscular Junctions. In:  "Crustacean Nervous System" (ed. K. Wiese), Springer-Verlag , Berlin, pp. 248-265.

16. Atwood, H.L. (2002) The Crustacean Synapse Scene at the End of the Millenium. In: "Crustacean Experimental Systems in Neurobiology" (ed. K. Wiese), Springer-Verlag, Berlin 169-174.

17. Atwood, H.L. and Karunanithi, S. (2002) Diversification of synaptic strength: Presynaptic elements. Nature Reviews Neuroscience 3: 497-516.